0 & W 1988
'2DEC
Bulletin of the
British Museum (Natural History)
The Hemiuridae (Digenea) of fishes from the north-east Atlantic
David I. Gibson & Rodney A. Bray
Zoology series VolSl No 1 30 October 1986
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'or Id List abbreviation: Bull. Br. Mus. not. Hist. (Zool.)
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ISBN 0565 050230 ISSN 0007-1 498
British Museum (Natural History) Cromwell Road London SW7 5BD
Zoology series
VolSl No. 1 pp 1-125
Issued 30 October 1986
-2DEC1986
PRESENTED ! GENERAL
The Hemiuridae (Digenea) of fishes from the north-east Atlantic
David I. Gibson & Rodney A. Bray
Department of Zoology, British Museum (Natural History), Cromwell Road, London SW7 5BD
Contents
Synopsis
Introduction
Materials and methods . . . .
Systematic section
Family Hemiuridae . . .
A taxonomic history of the group . Life-history and larval records Key to the subfamilies . Subfamily Hemiurinae Hemiurus appendiculatus Hemiurus communis Hemiurus levinseni . . Hemiurus luehei .... Parahemiurus . . Subfamily Dinurinae
Dinurus ..... Ectenurus lepidus . . . Subfamily Elytrophallinae Lecithocladium excisum Subfamily Glomericirrinae
Glomericirrus macrouri Subfamily Lecithochiriinae Lecithochirium rufoviride Lecithochirium furcolabiatum Lecithochirium fusiforme . •. Lecithochirium musculus Br achy phallus crenatus . Subfamily Plerurinae
Dinosoma ventrovesicularis sp. nov. Synaptobothrium caudiporum Host-parasite list . . . . .
Acknowledgements
References
1 13 25 31 38 38 38 39 45 45 54 55 61 62 69 76 83 90 97 97 103 107 111 111
Synopsis
Keys, original descriptions, full host-records, locality data and comments on some aspects of their biology are presented for all of the hemiurid species recorded from the north-east Atlantic region. The species described are Hemiurus appendiculatus, H. communis, H. levinseni, H. luehei, Ectenurus lepidus, Lecithocladium excisum, Glomericirrus macrouri, Lecithochirium rufoviride, L. furcolabiatum, L. fusiforme, L. musculus, Brachyphallus crenatus, Dinosoma ventrovesicularis sp. nov. and Synaptobothrium caudiporum. In addition, details of the records of the larval stages from invertebrates are given, and comments are made
Bull. Br. Mus. not. Hist. (Zool.) 51 (1): 1-125
Issued 30 October 1986
2 D. I. GIBSON & R. A. BRAY
on the presence in the region of species of the genera Parahemiurus and Dinurus. The work includes numerous new host-records and a complete host-parasite check-list for the region.
Lecithocladium cristatum is considered a valid species, but L. crenatum is believed to be a questionable synonym of L. excisum. A great reduction in the number of the accepted species of Lecithocladium occurring in the Indian Ocean region is proposed. Sterrhurus and Ceratotrema are considered synonyms of Lecithochirium, and L. furcolabiatum is shown to be a valid species. L. gravidum is treated as a synonym of L. rufoviride, but L. grandiporum is, for the present, retained as distinct from L. fusiforme. Dinosoma ventrovesicularis sp. nov. is described from the deep-water fish Xenodermichthys socialis.
Introduction
This is the fourth in a series of papers on the helminth-fauna of fishes from the north-east Atlantic region (see Bray & Gibson, 1977, 1980; Gibson & Bray, 1977) and the third to deal with hemiuroid groups. The Hemiuridae is a group of digeneans which usually occurs in the stomach of marine teleosts, although forms are known from freshwater teleosts and the lung of piscivorous sea-snakes. These worms are unique in that they possess a terminal ecsoma or 'tail', which is capable of being retracted within the body (soma). This structure is thought to be associated with the inhospitable environment (the cardiac stomach, which these worms inhabit) in that it is believed to be a feeding organ protruded only when the pH and/or osmolarity are suitable (Gibson & Bray, 1979). The hemiurid conception and classification used in this contribution follows that of Gibson & Bray (1979).
Materials and methods
The materials and methods used in this investigation and the areas of study are as outlined by Bray & Gibson (1977). The collecting trips undertaken are as reported in previous contributions in this series, but also include: the northern North Sea and off northern Scotland aboard the MAFF RV Cirolana in 1979, the DAFS RV Explorer in 1982 and 1983 and the DAFS RV Scotia in 1984 (by R.A.B.); the Bay of Biscay aboard the MAFF RV G. A. Reay in 1980 (by R.A.B.); at Kristineberg Biological Station, Sweden, in 1976 (by D.I.G.); at the University of Troms0, Norway, in 1980 (by D.I.G.); at the M.B.A. Laboratory, Plymouth, in 1980 (by R.A.B.); at the Marine Biological Laboratory, Helsinger, Denmark, in 1981 (by D.I.G.); at the Marine Labora- tory and Huntsman Laboratory, St Andrews, New Brunswick, in 1982 and 1984, respectively (by R.A.B.); and at the Pacific Biological Station, Nanaimo, British Columbia, in 1982 (by D.I.G.). The morphological terminology used follows that of Gibson & Bray (1979), and the fish nomenclature and classification used usually follows Hureau & Monod (1973) and Nelson (1976), respectively.
Systematic section Family HEMIURIDAE Looss, 1899
Lecithochiriidae Liihe, 1901.
Dinuridae Looss, 1907.
Elytrophallidae Skrjabin & Guschanskaja, 1954.
DIAGNOSTIC FEATURES. Body usually small, but elongate. Ecsoma present, occasionally reduced or vestigial. Body-surface unspined, smooth or with annular plications; the latter occasionally being crenulate, giving a scaly appearance. Presomatic pit or ventro-cervical groove occasionally present. Oral and ventral suckers well developed; usually close together. Prepharynx absent. Pharynx well developed. Oesophagus usually short. 'Dnisenmagen' normally present. Gut-caeca terminate blindly, usually within ecsoma. Testes two; tandem, oblique or symmetrical; pre- ovarian; in hindbody. Seminal vesicle tubular, saccular or constricted into portions; muscular
HEMIURIDAE 3
or thin-walled; in fore- or hindbody. Pars prostatica of variable length; usually tubular, but occasionally vesicular; may be linked to seminal vesicle by aglandular duct. Ejaculatory duct, if present, usually short. Sinus-sac usually well developed, occasionally reduced or absent. Prostatic or ejaculatory vesicle occasionally present within sinus-sac. Hermaphroditic duct usually enclosed within sinus-sac. Permanent sinus-organ and genital atrium well developed, small or absent; temporary sinus-organ may form from hermaphroditic duct in some cases. Genital pore mid- ventral at level of oral sucker or pharynx. Ovary oval; usually entire; post-testicular. Mehlis' gland post-ovarian. Laurer's canal and canalicular or blind seminal receptacle absent. Juel's organ and uterine seminal receptacle present. Uterus coiled mainly in pre- and/or post-ovarian region of hindbody; few or no coils present in forebody; initially descending into or towards ecsoma and then ascending towards forebody. Eggs numerous; small; embryonated; rarely with a polar filament. Vitellarium varies between forms with seven tubular branches (three on one side of body, four on other) and forms with two distinct, oval masses; mainly post-ovarian. Excretory vesicle Y-shaped; arms united in forebody or not. Parasitic mainly in gut, especially stomach, of marine teleosts; occasionally present in gut of freshwater teleosts and lung of sea-snakes.
A taxonomic history of the group
Details of the taxonomic history of the hemiuroid digeneans have been reviewed by Gibson & Bray (1979). The family-group based on Hemiurus Rudolphi, 1809, was originally erected by Looss (1899) as a subfamily and raised to the family-level by Luhe (190 la). In early works on the Hemiuridae, a wide range of dissimilar forms were included in this family. Fuhrmann (1928), for example, included the Hemiurinae, Derogeninae, Dinurinae, Lecithasterinae, Sclerodistominae and Sterrhurinae ( = Lecithochiriinae) within the Hemiuridae. Such a wide conception of the family has, even recently, been very popular. Workers, such as Manter & Pritchard (1960a) and Yamaguti (1971) have included all of these forms, with the exception of the sclerodistomines, within the Hemiuridae. Although some of these groups, such as the Derogeninae ( = Halipeginae), have at various times been removed from the Hemiuridae, it was not until the works of Skrjabin & Guschanskaja (1954, I955a,b, 1956) that a major change occurred. These authors retained the Hemiuridae for only the Hemiurinae and the Aphanurinae, and they recognized the Dinuridae, Lecithasteridae, Lecithochiriidae, Elytrophallidae and the Halipegidae. This system, although not accepted in its entirety, was given some support by La Rue (1957) and Joyeux & Baer (1961), who recognized the Dinuridae, Halipegidae, Lecithasteridae and Lecithochiriidae, the latter authors including only the Hemiurinae and the Prosorchiinae within the Hemiuridae. Recently, in their revision of the Hemiuroidea, Gibson & Bray (1979) have taken an intermediate position and restricted the Hemiuridae to ecsomate forms, thus recognizing the Derogenidae ( = Halipegidae), Lecithasteridae and Sclerodistomidae as being distinct, and transferring the Aphanurinae to the Bunocotylidae. Within the Hemiuridae these authors accepted the following subfamilies: Hemiurinae, Dinurinae, Elytrophallinae, Glomericirrinae, Hypohepaticolinae, Lecithochiriinae, Lethadeninae, Plerurinae and Pulmoverminae. This version of the classification is followed in the present work.
Life-history and larval records
No typical hemiurid life-histories are fully known, but it is likely that they follow the typical hemiuroid pattern, as described by K0ie (1978, 1979) for the derogenid Derogenes varicus (M tiller, 1780). Embryonated eggs passed by the fish in its faeces are swallowed by gastropod molluscs and hatch in the gut, releasing the miracidium. Within the tissues of the mollusc the miracidium is transformed into a mother-sporocyst which normally gives rise to a generation of rediae (on rare occasions daughter-sporocysts). Within these parthenitae develop cystophorous cercariae, peculiar and highly modified forms possessing a tail with a caudal cyst into which the body of the worm can be withdrawn and a delivery tube through which the cercarial body is injected into the second intermediate host after the cercaria is released from the mollusc. The metacercaria, which is unencysted, usually occurs in the haemocoel of planktonic organisms, such as copepods and chaetognaths. Judging from K0ie's (1978) work on D. varicus, it seems that
4 D. I. GIBSON & R. A. BRAY
chaetognaths acquire the parasites by feeding upon infested copepods, but it is not known for certain that hemiurids cannot be acquired directly by these hosts. The piscine definitive hosts acquire these parasites either directly, in the case of young fish, small fish and filter-feeders, or indirectly by feeding upon small infested fishes. In some cases, such as some lecithochiriines, immature forms may occur encapsulated in the body-cavity of fishes which appear to act as obligatory third intermediate hosts. The complete life-history of Lecithochiriumfurcolabiatum, as deciphered by Matthews (1980, 198 la, b, 1982a), is discussed on p. 71.
Since all hemiuroids appear to have cystophorous cercariae, it is usually difficult to recognize those of hemiurids (sensu strict o). Many of the records of cercariae and metacercariae were published when the systematics of the group were even less well understood, and so many are questionable. All early records of ecsomate metacercariae, for example, were referred to as 'Distoma appendiculatcC ; but it is unlikely that many, or indeed any, were Hemiurus appendiculatus (Rud., 1802). Moreover, some of the cercariae probably refer to other hemiuroid groups. Such records from the north-east Atlantic region include the following:
CYSTOPHOROUS CERCARIAE*
Cercaria appendiculata Pelseneer, 1906
( = Derogenes various) Natica alderi-see Pelseneer (1906), Vaullegeard (1896), Dollfus (1950) and K0ie (1979).
Cercaria sp. of Rees, in Dollfus (1950)
Natica alderi and N. catenata. Plymouth, Devon, England. Rees, in Dollfus (1950; possibly identical with Cercaria appendiculata).
Cercaria bunocotyle progenetica (Markowski, 1936)
( = Bunocotyle progenetica) Hydrobia ulvae. English Channel and Atlantic coast of France. Deblock (1975).
Cercaria K of Rothschild (1936)
Hydrobia ulvae. Plymouth, Devon, England, and Scotland. Rothschild (1936). Possibly Bunocotyle according to Deblock (1975, 1981).
Cercaria sinitzini Rothschild, 1938 Hydrobia ulvae. St. John's Lake near Plymouth, Devon, England, and Scotland. Rothschild (1938a, b).
— Atlantic coast of France. Deblock (1981).
Cercaria dollfusi Arvy, 1951 Philine aperta. Dinard, Ile-et-Vilaine, France. Arvy (1951).
Cercaria sp. of Francois, in Pelseneer (1906).
Philine aperta. Fouras, Charente-Maritimes, France. Francois, in Pelseneer (1906). Not C. dollfusi according to Arvy (1951).
Cercaria melanocystea Arvy & Gaillard, 1956 Pandora albida. Dinard, Ile-et-Vilaine, France. Arvy & Gaillard (1956).
Cercaria prenanti Arvy, 1949 Dentalium entails. Dinard, Ile-et-Vilaine, France. Arvy (1949aA 1957).
Cercaria calliostomae Dollfus, 1923 Calliostoma zizyphinum. Roscoff, Finistere, France. Dollfus (1923).
— Plymouth, Devon, England. Matthews (1982a,£).
*See also Timofeeva (1976) for forms from the Barents Sea.
HEMIURIDAE 5
Cercaria vaullegeardi Pelseneer, 1 906
( = Lecithochiriwn (?) rufoviride)
Gibbula cinerea. Wimereux, Pas-de-Calais, France. Pelseneer (1906). Gibbula umbilicalis. Isles Chausey, Gulf of St Malo, English Channel. Gaillard (1953).
— Roscoff, Finistere, France. Arvy (1964).
- Sandy Haven, Pembrokeshire, Wales. James, in Popiel (1976), Popiel (1976, 1978).
Cercaria vaullegeardi Pelseneer of Matthews
( = Lecithochirium furcolabiatum)
Gibbula umbilicalis. Plymouth, Devon, England. Matthews (1980, 1981a,6, 19826), Gibson, Rollinson & Matthews (1985).
Cercaria filamentosa Reimer, 1971
(? '= Brachyphallus crenatus) Rissoa membranacea. Western Kattegat, Denmark. K0ie (1983).
METACERCARIAE IN PLANKTON
COPEPODA
Acartia clausii [body-cavity] Plymouth Sound, Devon, England. (May, February) Lebour (1923; as Hemiurus communis) and (June) Lebour (1935; as H. communis).
- [body-cavity and carapace] Roscoff, Finistere, France. Rose, in Dollfus (1923; not named); Rose (1925; as Apoblema).
— [haemocoel] Boulogne, English Channel. Canu (1892; as Apoblema appendiculatum).
— [?] Brackish water at Alnmouth, Northumberland, England. Brady (1900; as 'immature trematode'). [?] Firth of Clyde, Scotland. Marshall (1925; as H. appendiculatus).
Acartia sp. [body-cavity] North Sea (or nearby waters). Apstein (191 1; as Distomum appendiculatum). Calanus finmarchicus [body-cavity] North Sea (or nearby waters). Apstein (191 1; as D. appendiculatum}. Calanus sp. [?] Firth of Clyde, Scotland. Marshall (1925; as H. appendiculatus). Centropages hamatus [body-cavity] North Sea (or nearby waters). Apstein (191 1; as D. appendiculatum).
— [?] Kiel Bay, N Germany (February). Giesbrecht (1882; see Monticelli, 1891). — [?] Roscoff, Finistere, France. Rose, in Dollfus (1923; not named).
Centropages typicus [?] Roscoff, Finistere, France. Rose, in Dollfus (1923; not named).
Paracalanus parvus [body-cavity] Boulogne, English Channel. Canu (1892; as Apoblema appendiculatum).
[body-cavity] ? Helgoland, North Sea. Claus (1863; as Monostomum: see Steuer, 1928).
Pseudocalanus elongatus [body-cavity] North Sea (or nearby waters). Apstein (191 1; as D. appendiculatum).
— [?] Kiel Bay, N Germany. Pratt (1898; as Apoblema appendiculatum). (February) Giesbrecht (1882: see Monticelli, 1891).
Pseudocalanus sp. [cercaria observed to penetrate] Plymouth, Devon, England. Rees, in Dollfus (1950; as
Cercaria sp. ( = Derogenes)). Temora longicornis [?] Roscoff, Finistere, France. Rose, in Dollfus (1923; not named).
— [body-cavity] North Sea (or nearby waters). Apstein (191 1; as D. appendiculutum).
Tigriopsis brevicornis [body-cavity] Wembury Bay, Devon, England. Matthews (19826; as 'hemiurid meta- cercariae' naturally: experimental infestations with Cercaria vaullegeardi -see Matthews, 19816, 19826). Copepod [?] Kiel Bay, N Germany. Mobius, in Willemoes-Suhm (1871; as Distoma ocreatum).
CIRRIPEDIA
Balanus balanoides [cercaria observed to penetrate] Plymouth, Devon, England. Rees, in Dollfus (1950; as Cercaria sp. (? = Derogenes)).
CHAETOGNATHA
Sagitta elegans [body-cavity] Northumberland, England. Meek (1928; as Hemiurus communis).
(?) Sagitta rostrata [?] Orkney Isles. Busch (1851; as Distoma crassicaudatum - see Lebour 1917; Dollfus,
1960a).
Sagitta setosa [body-cavity] Northumberland, England. Meek (1928; as H. communis). (?) - - [?] In region of North Sea and English Channel (see Dollfus, 1960a). Busch (1851; as D.
crassicaudatum - see Lebour, 1917; Dollfus, 1960a).
D. I. GIBSON & R. A. BRAY
[?] Helgoland, North Sea. Leuckart & Pagenstecher (1858; as Distoma-see Dollfus, 1960a).
Sagiita sp. [gut near anus and anterior to caudal septum] St Andrews, Fife, Scotland (January, February). Mclntosh (1889; as 'trematode': ?Derogenes, according to Dollfus, 1960a).
— [towards posterior part of body and elsewhere] Firth of Clyde, Scotland. Scott (1896; as 'distoma': resembles Lecithaster).
Spadella cephaloptera [?] Roscoff, Finistere, France (August). Dollfus (1960a; as (?) Lecithaster or Lecithochirium).
PROTOZOA
(?) Noctiluca sp. [?] Concarneau, Brittany, France. Pouchet (1883); Pouchet & de Guerne (1887).
CTENOPHORA
Pleurobrachia pileus [gut] Galway, Eire. Collected by S. Y. Yip. BM(NH) Reg. No. 1978. 12.18.1-2; as Hemiurus (?) communis. Yip (1984; as H. communis).
— [?] Northern 0resund, Denmark. K0ie (1983; as Brachyphallus crenatus).
ANNELIDA
Polygordius sp. trochophore larva [external] Plymouth, Devon, England. Lebour (1935; as H. communis).
FREE-LIVING METACERCARIAE
See: Giesbrecht (1882; Kiel Bay); Meek (1928; Northumberland, England); Monod, in Dollfus (1923; Concarneau, Brittany, France); and Lebour (1935; Plymouth, Devon, England).
Key to the subfamilies of the Hemiuridae in the north-east Atlantic
(In order to use this key it may be necessary to section the material.)
1 Ejaculatory (prostatic) vesicle present within sinus-sac, occasionally partly external (the vesicle
should not be confused with the pars prostatica, which may be vesicular) .... 2 Ejaculatory (prostatic) vesicle absent 3
2 Long, convoluted hermaphroditic duct and thin-walled permanent sinus-organ present; seminal
vesicle bipartite, anterior part muscular; vitellarium two irregularly oval masses .
* . . GLOMERICIRRINAE (p. 54)
Hermaphroditic duct relatively straight; permanent sinus-organ absent; seminal vesicle tubular or saccular and partitioned, usually thin-walled; vitellarium seven digitiform to oval lobes or with tendency to form two distinct, often lobed, masses; ecsoma sometimes reduced or apparently absent. ... .... LECITHOCHIRHNAE (p. 61)
3 Sinus-sac absent or poorly developed, when present usually of 'open'-type; seminal vesicle
entirely or mainly thin-walled, usually constricted into portions; ecsoma sometimes poorly
developed PLERURINAE (p. 97)
Sinus-sac present, usually well developed, occasionally small ... .4
4 Vitellarium two symmetrical to slightly oblique, entire or lobed masses HEMIURINAE (p. 6) Vitellarium seven distinct oval to tubular lobes 5
5 Seminal vesicle with thick muscular wall, oval; permanent sinus-organ normally delicate and
amuscular . ELYTROPHALLINAE (p. 45)
Seminal vesicle thin-walled and oval, tubular or constricted into portions; permanent sinus- organ large and muscular, reduced to small papilla or apparently absent .... . DINURINAE (p. 38)
Subfamily HEMIURINAE Looss, 1899
DIAGNOSTIC FEATURES. Ecsoma well developed. Body-surface plicated or 'scaly' (i.e. with crenulate plications). Presomatic pit absent. Testes tandem to oblique. Seminal vesicle thin- walled, or partly or slightly muscular; bipartite or oval; in hindbody. Pars prostatica tubular; long; gland-cells occasionally delimited by membrane. Sinus-sac present; often tubular; not enclosing ejaculatory (prostatic) vesicle. Permanent sinus-organ absent, but hermaphroditic duct may be protruded to form temporary sinus-organ. Genital atrium usually small, but variable in
HEMIURIDAE
length. Ovary oval. Vitellarium composed of two distinct oval masses, but these may show a slight tendency towards lobation (three lobes on one mass, four on the other). Excretory arms united in forebody. Parasitic in stomach of marine teleosts.
Genus HEMWRUS Rudolphi, 1809
Apoblema Dujardin, 1845.
Pronopyge Looss, 1899 (see Gibson & Bray, 1979:73; Bray & Gibson, 1980: 254).
Metahemiurus Skrjabin & Guschanskaja, 1954.
DIAGNOSTIC FEATURES. Body-surface with normal plications. Seminal vesicle constricted into two portions (? occasionally three), one of which may have a thick, muscular wall.
TYPE-SPECIES. Hemiurus appendiculatus (Rudolphi, 1802) [by subsequent designation: Stiles & Hassal, 1898].
Key to the species of Hemiurus recorded from the north-east Atlantic
1 Sucker-ratio normally 1 : < 1-1; distribution arctic-boreal; parasitic mainly in gadoids, but also
occurs in other groups, such as salmonids and flatfishes H. levinseni (p. 25) Sucker-ratio normally 1 : >l-5 2
2 Seminal vesicle relatively close to ventral sucker; distribution boreal; parasite in wide range of
marine teleosts, but especially common in gadoids . . . . H. communis (p. 13) Seminal vesicle well posterior to ventral sucker; distribution Lusitanean; primarily parasites of clupeids 3
3 Dorsal plications reach back to level of seminal vesicle or testes (in well-preserved material);
parasite of clupeids, such as herring, sprats and pilchards, and their predators (further
differences are outlined in the text) H. luehei(p. 31)
Dorsal plications do not reach back to the level of the caecal bifurcation (except in very small specimens); parasites of Alosaspp H. appendiculatus (p. 7)
Hemiurus appendiculatus (Rudolphi, 1802) Looss, 1899
? Fasciola alosae Hermann, 1783.
? Fasciola clupeae Schrank, 1788.
? Distoma clupeae (Schrank) Zeder, 1803.
? Distoma clupeae rhenanae Rudolphi, 1809.
Fasciola appendiculata Rudolphi, 1802, nee Frolich, 1802.
Distoma appendiculatum (Rudolphi) Rudolphi, 1809, nee Leidy, 1877.
Distoma appendiculatum of various authors (in part).
Distoma (Apoblema) appendiculatum (Rudolphi) Dujardin, 1 845 (in part).
Apoblema appendiculatum (Rudolphi) Dujardin sensu Blanchard (1847).
Distoma ventricosum Rudolphi, 1819 (nee Fasciola ventricosa Pallas, 1774) of Wagener (1860) (in part).
TYPE-HOST AND LOCALITY. Alosa alosa, Griefswald on Baltic coast of East Germany. RECORDS
(i) Material studied
(a) From the NE Atlantic
Alosa alosa [stomach] Locality unknown. Material purchased from C. T. E. von Siebold in 1851. BM(NH)
51.7.24.180. (see Baird, 1853: 54; as Distoma (Apoblema) appendiculatum). Alosa fallax [stomach] Off St. Kilda. Collected by Z. Kabata. BM(NH) 1963.6.21.44-^8.
- [stomach] SW Barra Head, Scotland (56°N, 08°W; depth 170 m; July, 1954). BM(NH) 1959.10.14.4-6. (Material of Williams, 1960: 708).
- [stomach] Bay of Biscay (44°N, 08°W; depth 252-304 m; Jan., 1971). BM(NH) 1973.5.17.60-62. (Material of Bray, 1973: 178).
- [stomach] Whitby, Yorkshire, England. Collected by G. A. Boxshall. BM(NH) 1976.1.5.61.
[?] River Severn (below Gloucester), England (May). Collected by C. R. Kennedy. BM(NH)
1983.10.19.5-6.
D. I. GIBSON & R. A. BRAY
- [?] Den Oever, Netherlands (Sept., 1960). Zoological Museum, Amsterdam. Cat. no. V.P1. 372.1. (Material of Willemse, 1968: 84).
— [?] Texel, t'Horntje, Netherlands (April, 1962). Zoological Museum, Amsterdam. Cat. no. V.P1. 403.1. (Material of Willemse, 1968: 84).
- [stomach] Scotland. Collected by K. MacKenzie. BM(NH) 1983.1 1.16.1-7.
- [stomach] Portuguese coast (42°N, 08° W; March 1968). Laboratoria de Helminthologia Collection, Institute Oswaldo Cruz, Rio de Janeiro. Cat. no. 30.632a-b. (Material of de Oliveira Rodrigues el al., 1972: 90).
- [stomach] Off Scarborough, North Yorkshire, England (Sept., 1976; Dec., 1976; Dec., 1977; Jan., 1978; Nov., 1978; March, 1979). Collected by D. Whittaker. BM(NH) 1982.1.19.1-3 and 1982.10.19.7-102.
— [stomach] Estuary of River Severn off Lydney, Gloucestershire, England (May, 1979). Collected by M. V. Aprahamian. BM(NH) 1980.6.20.1-8.
- [?] Oslofjord, Norway (1868). Collected by Esmark. Zoological Museum, Oslo. Reg. No. C.62.
(b) From elsewhere
Alosafallax [stomach] Cairo, Egypt. Material of A. Looss. BM(NH) 1931.10.7.35-40.
(ii) NE Atlantic records from the literature
(?) Alosa alosa [intestine] Rennes, Brittany, France. Dujardin (1845: 420; as Distoma (Apoblema)
appendiculatum).
(?) [stomach] Belgian coast, van Beneden (1871: 69; as Distoma appendiculatd).
(?) [gut] River Rhine at Basle, Switzerland. Zschokke (1896: 775; as Distoma ocreatum).
— [stomach] Portuguese coast (March, 1954). Tendeiro & Valdez (1955: 55). (?) Alosa (?) fallax [intestine] River Rhine (May). Hermann (1783: 46; as Fasciola alosae). (?) Alosafallax [stomach] Belgian coast, van Beneden (1871: 68; as Distoma appendiculatd).
- [?] Locality not given. Odhner (1905: 349, footnote).
- [stomach] Atlantic W of Scotland (July, 1954). Williams (1960: 708).
- [?] Den Oever (Sept., 1960) and Texel, t'Horntje (April, 1962), Netherlands. Willemse (1968: 84).
- [stomach] Portuguese coast (42°N, 08° W; March, 1968). de Oliveira Rodrigues et al. (1972: 90).
- [stomach] SW Bay of Biscay (44°N, 08°W; depth 252-304 m; Jan., 1971). Bray (1973: 178).
ASPECTS OF BIOLOGY. The life-history of this species is not known, but it presumably follows a similar pattern to that of many other hemiurids, i.e. egg, miracidium - becoming transformed into a mother-sporocyst (in a marine mollusc), redia, cystophorus cercaria, metacercaria (in a planktonic invertebrate, especially copepods and chaetognaths), and adult (in the stomach of marine fishes, in this case Alosa spp.). The molluscan host is unknown. There have been many records in the literature indicating the nature of the second intermediate host, but most of these are from the late 19th and early 20th centuries, before the systematics of the genus were under- stood. Although most of these records were attributed to Hemiurus (or Distoma) appendiculatus, it is almost certain that at least the majority of these really refer to the more common species of the genus or even to other hemiurid genera (see p. 4). More recently, Hunninen & Cable (1943) claim to have found the metacercaria of H. appendiculatus in the copepod Acartia off the coast of New England; but, as discussed below, there is little concrete evidence to indicate that this parasite occurs on the western side of the North Atlantic Ocean. Indeed, we consider that it has a Lusitanean distribution (Gibson & Valtonen, 1981; Gibson, 1982, 1983), and that its distribution is limited to that of its piscine hosts. Aspects of the seasonal prevalence of this species in Alosa fallax in Lake Jezero, Yugoslavia, are given by Kazic (1970).
H. appendiculatus appears to be restricted to Alosa alosa and to A. fallax in the north-east Atlantic region, and it especially prevalent in the latter. These hosts are fish which enter rivers in the spring and summer to spawn in freshwater. This accounts for the records of this parasite in rivers many miles from the sea. The cause of the recent paucity of records from A. alosa is prob- ably the marked decline in the numbers of this fish during the 20th century due to the pollution of many of the major European rivers. A. fallax has not declined to the same extent, as it does not normally penetrate nearly as far upstream.
PREVIOUS DESCRIPTIONS. Looss (1896: 131, as Apoblema appendiculatum; 1908: 103); Odhner (1905: 351, no figure); Tendeiro & Valdez (1955: 55, ignore figure). There are other descriptions;
HEMIURIDAE 9
but we have listed only the best original descriptions which we consider definitely refer to specimens of H. appendiculatus.
DESCRIPTION (Fig. 1). Unfortunately, we did not have available for study material collected by ourselves and fixed in glacial acetic acid or Berland's fluid. The following description is, there- fore, based upon specimens many of which are rather flattened, contracted or derived from frozen hosts.
The body of this worm, although very variable, reaches a greater size than the other species of the genus in the NE Atlantic region. It is subcylindrical, narrowing terminally; but its length- width ratio depends greatly upon the extent to which the ecsoma is protruded (Fig. 1 A & B). The latter structure can be completely withdrawn or occupy up to half of the total length of the worm. Measurements of this species are given in Table 1 . The body-surface, with the exception of the ecsoma, is covered with annular plications ventrally and laterally. These tend to become less distinct towards the posterior end of the body-proper (soma). Dorsally, the plications tend not to occur posteriorly to the level of the intestinal bifurcation or even the pharynx; but in some cases they disappear altogether, while in some small specimens a small region of plications may occur dorsally just posterior to the ventral sucker. The oral sucker is ventrally subterminal and sur- mounted by a small pre-oral lobe. The ventral sucker is situated close to, and is about one and a half to two times the size of, the oral sucker, the ratio usually being in the region of 1 : 1 -6-2-1.
There is no prepharynx, but a muscular, oval pharynx gives rise to a short, cylindrical to globular oesophagus with a tegumental lining. The oesophagus passes postero-dorsally and divides to form two short, laterally oriented ducts, which lead into distinct 'Driisenmagen' ('glandular stomachs'). The two caeca pass back in the dorso-lateral fields from these organs and terminate blindly almost at the posterior extremity of the ecsoma.
The excretory pore occurs terminally on the ecsoma. It leads into a tubular, Y-shaped excretory vesicle which bifurcates at about a level just posterior to the seminal vesicle. The stem passes forward medially and slightly dorsally and the arms pass into the forebody ventro-laterally before uniting postero-dorsally to the oral sucker.
The two oval testes occur ventrally in the hindbody, usually about midway between the ventral sucker and the ovary; but this relationship is variable, depending upon the state of contraction. They are usually arranged obliquely, with the right testis more anteriorly situated, but they are sometimes symmetrical or their position may be reversed. The seminal vesicle consists of two oval, contiguous lobes, and occurs closely anterior or antero-dorsal to the testes. The proximal lobe is normally the larger, sometimes being larger than the testes; but it is thin-walled and on some occasions difficult to distinguish. The distal lobe, which leads directly into the pars prostatica, has a relatively thick, muscular wall. The pars prostatica is very long, winding in the space between the seminal vesicle and the ventral sucker, before passing into the forebody, directly or sinuously, to join the sinus-sac a short distance in front of the anterior margin of the ventral sucker (Fig. 1C). This duct is relatively dilate with a sparse, narrow covering of external gland-cells and a lining of anuclear protrusions (blebs). Spermatozoa can be seen in the lumen of the pars prostatica in one sectioned specimen. There appears to be a very short ejaculatory duct which is the small region of the male duct distal to the pars prostatica, that passes through the wall of the sinus-sac and unites with the metraterm to form an hermaphroditic duct. This union occurs just within the sinus-sac (Fig. 1C). The sinus-sac is tubular, straight to slightly sigmoid in the dorso-ventral plane, and possesses a thick, muscular wall. It contains the long, tubular hermaphroditic duct. In the sectioned specimen the wall of the proximal third of this duct appears to be formed from a thick layer of circular and longitudinal muscles, the middle third has a thin, smooth wall except for a small region lined with what appear to be detachable globules similar to those described below in Hemiurus communis, and the wall of the distal third is lined with a close-packed arrangement of tegumental, papillate structures. The latter region presum- ably forms a temporary sinus-organ during copulation, the papillate structures probably being an analogue of the spines which occur on the cirrus of some groups. In some fixed specimens this latter part of the hermaphroditic duct is sometimes partly everted, in some cases extending
10
D. I. GIBSON & R. A. BRAY
B
Fig. 1 Hemiurus appendiculatus ex Alosa fallax. (A,B) Entire worm, flattened and distorted; (C) Sagittal section of forebody. Scale bars: A,B 1 mm; C 200 fan.
HEMIURIDAE Table 1 Measurements of Hemiurus appendiculatus
11
|
Authority |
Material of |
Looss (1908) Tendeiro & |
Present material |
|
Looss (1986) |
Valdez(1955) |
||
|
in BM(NH) |
|||
|
Host |
Alosafallax |
Alosafallax Alosa alosa |
Alosafallax* |
|
Locality |
River Nile at |
? Portuguese |
NE Atlantic |
|
Cairo |
coast |
region |
|
|
Length (mm) |
1-3^-3 |
3^ 3-00-5-65 |
0-75-6-70 |
|
plus ecsoma |
|||
|
Breadth (mm) |
0-21-0-501 |
0-4-0-5 0-76-1-29 |
0-20-1-00 |
|
Ecsoma (mm) |
0-45-1-8 |
0-04-1-21 |
0-00-2-25 |
|
Ecsoma/body- |
35-42 |
(1-24) |
0-47 |
|
length (%) |
|||
|
Forebody (mm) |
0-15-0-27 |
0-66-1-03 |
0-13-0-75 |
|
Oral sucker (mm) |
0-08-0- 13 x |
c. 0-2 diam. 0-1 7-0-36 x |
0-075-0-22 x |
|
0-10-0-17t |
0-18-0-31 |
0-08-0-28 |
|
|
Ventral sucker |
0-1 7-0-32 x |
c. 0-4 diam. 0-36-0-67 x |
0-14-0-51 x |
|
(mm) |
0-16-0-28f |
0-36-0-71 |
0-14-0-53 |
|
Sucker-ratio |
1: 1-6-1 -65f |
1:2 (1:1-94-2-45) |
1 : 146-2-15 |
|
Seminal vesicle to |
12-14 |
- — |
9-22 |
|
ventral sucker/ |
|||
|
body-length (%) |
|||
|
Testes (mm) |
7-0- 13x7-0- 13 |
0-1 2-0-3 Ix |
0-02-0-27 x |
|
0-10-0-32 |
0-02-0-27 |
||
|
Ovary (mm) |
7-0- 10x7-0- 17 |
0-14-0-32 x |
0-025-0-22 x |
|
0-18-0-34 |
0-08-0-29 |
||
|
Vitelline masses |
0-06-0-20 x |
0-1 3-0-38 x |
0-08-0-33 x |
|
(mm) |
0-11-0-20 |
0-12-0-34 |
0-04-0-25 |
|
Eggs (jim) |
22x10 |
20-23 x 10-12 18-24 x 10-12 |
18-27 x 8-12 |
(USUALLY 22-24 x 10)
Measurements in parentheses are calculated from figures. ""Includes one specimen from Alosa alosa. fMeasurements from specimen mounted laterally.
through the genital pore. There is a small genital atrium which opens to the exterior mid- ventrally close to the base of the ventral margin of the oral sucker.
The subglobular ovary is present in a position between the middle and posterior end of the soma, or even within the ecsoma, its position depending upon the extent of the contraction of the body and the extent to which ecsoma is evaginated. It is well separated from the testes by loops of the uterus. The ovarian complex is very compact and the ducts are very difficult to follow in our sectioned specimen. A well-developed Juel's organ, Mehlis' gland and uterine seminal receptacle are, however, clearly visible in sections postero-dorsal to the ovary. The arrangement of these organs and the associated ducts is presumably similar to that which we have described in detail for Hemiurus levinseni (see p. 30). The uterine seminal receptacle is large and winds posteriorly to the vitellarium. The uterus continues back, following a convoluted course into the ecsoma, and, when the latter is evaginated, often reaches into the posterior half and occasionally into the posterior third of this organ. It then reflexes and winds anteriorly, coiling especially between the ovary and the ventral sucker, where it is very broad, and particularly in the dorsal field and posterior to the testes where it fills much of the available space. At the level of the ventral sucker the uterus narrows, and runs forward directly or sinuously to the base of the sinus-sac. Immediately prior to its entry into the wall of the sinus-sac, there is some evidence in our sectioned specimen that there may be a slight constriction caused by a sphincter muscle (Fig. 1 C), which forms a small vesicle
12 D. I. GIBSON & R. A. BRAY
similar to the one described in Hemiurus communis (see p. 24). The numerous small eggs which fill much of the uterus are operculate and lack spines or filaments. The vitellariwn is composed of two oval masses which lie symmetrically positioned, ventral and immediately posterior to the ovary. In juvenile forms, however, these vitelline masses can be distinctly three- and four-lobed.
DISCUSSION Hemiurus appendiculatus was probably first reported, as Fasciola alosae, by Hermann (1783) in Alosafallax (i.e. a shad which was not A. alosd) from the River Rhine. These specimens appear to have be re-named Fasciola clupeae by Schrank (1788) and Distoma clupeae rhenanae by Rudolphi (1809). The latter author did indicate, however, that this species was probably a synonym of Distoma appendiculatum, which he had earlier (1802) described, as Fasciola appendi- culata, from Alosa alosa in the Baltic Sea. More recent authors have accepted this synonymy, but have retained the specific appellation appendiculatus because, whereas the descriptions of both Fasciola alosae and F. appendiculata are meagre, Rudolphi's type-specimens have been available for study in the Berlin Museum.
Unfortunately, prior to the work of Odhner (1905), all of the currently accepted species of Hemiurus from the north-east Atlantic region (with the exception of//, ocreatus ( = H. luehei) and certain other hemiurids) tended to be recorded under the specific name appendiculatus. Odhner recognized the four species, H . appendiculatus, H. communis, H. levinseni and H. luehei, which are included in the present work.* The initial use of the name Hemiurus appendiculatus (usually under the generic names Distoma and Apoblemd) in the early literature for this complex of species has caused a certain amount of confusion for later workers. Many authors appear to have ignored the comments of Looss (1908), who suggested that H. appendiculatus occurs only in Alosafallax, and have recorded it in a whole range of hosts. Certainly its morphological simi- larity with H. luehei is partly responsible for this, as is the basic similarity in gross morphology of many of the hemiurids. As an example, Willemse (1968) recorded H. appendiculatus from Salmo trutta, Osmerus eperlanus and Gasterosteus aculeatus in addition to Alosa fallax. We have examined this material and, although the specimens from A. fallax are indeed H. appendiculatus, the remainder of the material was Brachyphallus crenatus (Rud., 1802) with the exception of a single specimen from G. aculeatus which was Lecithaster gibbosus (Rud., 1802). It is also possible that Linton (1940), who described H. appendiculatus from Alosa [Pomolobus] spp. and several other hosts from off the coast of New England, might also have misled other North American workers into believing that this species occurs on the western side of the North Atlantic (our specimens from Alosa [ = Pomolobus] pseudoharengus in Passamaquoddy Bay, New Brunswick, are H. levinseni - see p. 26). We can find no concrete evidence that this species occurs outside European or North African (mainly Mediterranean) waters, both in the sea and freshwater, or in hosts other than Alosafallax and, less frequently, A. alosa. The records from Alosa [ = Caspialosa] spp. in the Black Sea should be carefully reconsidered in the light of our studies from the NE Atlantic. To return to Linton's record, the nature of the seminal vesicle and the shortness of the pars prostatica in his figures suggests that his material may have been Parahemiurus merus (Linton, 1910). On the other hand, the host-range is more similar to H. luehei than to H. appendiculatus; but, except for a record of Linton (1901) which we hesitate to accept, there are no records of H. luehei on the western side of the North Atlantic. Evidence from our own collections from the Atlantic coast of Canada (see Bray, 1979) and from the literature indicates that Hemiurus levinseni and Brachyphallus crenatus are the most widespread hemiurids in the region. In addition, material labelled H. appendiculatus from off Bermuda, which we have examined, is in our opinion a species of Parahemiurus Vaz & Pereira, 1930.
As suggested by Bray (1973), the figure of H. appendiculatus from Alosafallax off the coast of Portugal given by de Oliveira Rodrigues et al. (1972) differs somewhat from the usually accepted morphology of this species, especially in the nature and position of the seminal vesicle and pars
*Prior to Odhner's work, Wagener (1860) had recognized that a complex of ecsomate worms were known under the specific appellation appendiculatum. He split this into four species, one of which he referred to as Distoma ventricosum Rudolphi (in actual fact D. ventricosum Rud., 1819, is the type-species of Pronoprymna Poche, 1926-see Bray & Gibson, 1980). D. ventricosum of Wagener appears to be a composite of the modern concepts of//, appendiculatus and H. luehei.
HEMIURIDAE 13
prostatica. We initially thought that this material might belong to a species of Parahemiurus; but, through the kindness of Dr de Oliveira Rodrigues, we have examined some of this material and can confirm that they are typical specimens of H . appendiculatus.
Hemiurus communis Odhner, 1905*
Distoma appendiculatum (Rudolphi, 1802) of authors (in part). Distoma (Apoblemd) appendiculatum (Rudolphi) Dujardin, 1845 (in part). Apoblema appendiculatum (Rudolphi) Dujardin of authors (in part). Distoma ocreatum Molin of Olsson (1868) (in part). Hemiurus luehei of Duniec (1980).
TYPE-HOST AND LOCALITY. Salmo trutta** off Kristineberg, west coast of Sweden. RECORDS
(i) Material studied
(a) From the NE Atlantic
Ammodytes marinus [stomach] Aberdeen, Scotland (Oct., 1973). BM(NH) 1983.11.3.2.
Argentina sphyraena [?] Firth of Clyde, Scotland. BM(NH) 1966.9.6.26-30. (Material of Halliday, in Scott,
1969: 882). Aspitrigla cuculus [stomach] Plymouth, Devon, England (May, 1972). BM(NH) 1983.11.3.6-25.
- [stomach] Off west Scotland (57°N, 09°W; depth 120m; Oct., 1978). BM(NH) 1983.11.3.4.
- [stomach] N of Scotland (59°N, 04°W; depth 81 m; June, 1982). BM(NH) 1983.11.3.5. Ciliata mustela [stomach] Kristineberg, Sweden (Aug., 1976). BM(NH) 1983.11.3.6-25.
Conger conger [stomach] Off Banff, Scotland (45°N, 02°W; depth 152-1 86m; July, 1976). BM(NH) 1983.11.3.26.
- [stomach] Plymouth, Devon, England (May, 1932). BM(NH) 1932.11.29.1-6. (Material of Baylis & Jones, 1933: 631).
Cyclopterus lumpus [stomach] Aberdeen, Scotland. BM(NH) 1983.1 1.3.27.
Dicentrarchus labrax [stomach] Plymouth, Devon, England (Oct., 1972). BM(NH) 1983.11.3.28.
- [stomach] Aberdeen, Scotland (Jan., 1964). Collected by K. MacKenzie. BM(NH) 1983.11.3.29. Epigonus telescopus [stomach] NW of Flannan Isles (59°N, 09°W; depth 890-900 m; April, 1973). BM(NH)
1983.11.3.30.
Eutrigla gurnardus [stomach] Plymouth, Devon, England (Oct., 1972) BM(NH) 1983.11.3.31; (Oct., 1980) BM(NH) 1983. 11. 3.32.
- [stomach] NNE of Flannan Isles (59°N, 07°W; depth 104-108 m; July, 1976). BM(NH) 1983.1 1.3.33.
- [stomach] SE Ness Head, Scotland (58°N, 03°W; depth 62m; May, 1984). BM(NH) 1984.7.20.68. Gadus morhua [stomach] Oresund at Helsinger, Denmark (Aug., 1981). BM(NH) 1981.9.30.24.
- [stomach] Aberdeen, Scotland. BM(NH) 1972.3.27.9; (Feb., 1969) BM(NH) 1983.1 1.3.34; (Oct., 1973) BM(NH) 1983. 11. 3.35-38.
- [stomach] St. Andrews, Scotland (June, 1950). Collected by D. R. R. Burt. BM(NH) 1983.11.3.39.
- [stomach] Off Banff, Scotland (58°N, 02°W; depth 130-160 m; July, 1976). BM(NH) 1983.11.3.40-^2. -[stomach] Kristineberg, Sweden (Aug., 1976). BM(NH) 1983.11.3.43^9.
[stomach] Off E Scotland. (Isle of Fidra; 56°N, 03°W; depth 46m; May, 1984) BM(NH) 1984.7.20.63;
(Montrose Bank: 57°N, 02° W; depth 55 m; May, 1984) BM(NH) 1984.7.20.64. Gaidropsarus vulgaris [stomach] Scarborough, Yorkshire, England. (Dec., 1977) BM(NH) 1983.11.3.50-52;
(Jan., 1980) BM(NH) 1983.11.3.53; (Dec., 1981) BM(NH) 1983.11.3.54.
Gobius paganellus [stomach] Wembury, Plymouth, Devon, England (Oct., 1980). BM(NH) 1983.11.3.55. Hippoglossoides platessoides [stomach] Off eastern Scotland (56°N, 02°W; depth 65m; May, 1983).
BM(NH) 1983.1 1.3.56.
*Dollfus (1968: 148) lists Hemiurus serrulatus (Miiller, 1780) as a senior synonym of H. communis; but we have listed Mullet's record as a questionable synoynm of H. levinseni.
**Odhner (1905) did not list the hosts of this species, but Dollfus (19606) found specimens from both Salmo trutta and Raniceps raninus in Odhner's collection labelled as 'types'. Dollfus lists these as syntypes and, in addition, in a figure legend also refers to a specimen from Myoxocephalus scorpius as a syntype. As no distinct type-host has been put forward, we have listed it as Salmo trutta as Dollfus lists this host first, figures specimens from it in more detail, and because we have material from this host from the type-locality.
14 D. I. GIBSON & R. A. BRAY
Hippoglossus hippoglossus [stomach] Moray Firth (58°N, 03°W; depth 84m; June, 1982). BM(NH) 1983.11.3.57.
- [stomach] N of Scotland (59°N, 05°W; depth 64m; June, 1982) BM(NH) 1983.1 1.3.58; (59°N, 04°W; depth 55m; June, 1982) BM(NH) 1983.11.3.59.
Hoplostethus atlanticus [stomach] W of St. Kilda (58°N. 10°W; depth 920-980 m; April, 1973). BM(NH)
1983.11.3.56.
Hyperoplus lanceolatus [stomach] Aberdeen, Scotland (Oct., 1973). BM(NH) 1983.1 1.3.65-70. Limanda limanda [stomach] Cape Wrath, Scotland (59°N, 05°W; depth 90m; July, 1976). BM(NH)
1983.11.7.1.
- [stomach] Off Wick, Scotland (58°N, 03°W; depth 66-70 m; July, 1976). BM(NH) 1983.11.7.2.
- [stomach] Aberdeen, Scotland (Oct., 1973). BM(NH) 1983.11.7.3-8.
- [stomach] Moray Firth (58°N, 03°W; depth 35 m; June, 1982). BM(NH) 1982.1 1.7.9.
Lophius piscatorius [stomach] Plymouth, Devon, England. Collected by M. Rothschild, BM(NH) 1932.11.22.47-51; BM(NH) 1932.11.29.7-8 (Material of Baylis & Jones, 1933: 631).
- [stomach] N of Scotland (59°N, 04°W; depth 66m; June, 1982) BM(NH) 1983.11.7.12; Solan Bank (59°N, 05°W; depth 66m; May, 1984) BM(NH) 1984.7.20.67.
Merlangius merlangus [stomach] Stanton Banks, W of Scotland (56°N, 08° W; depth 165m; July, 1954) BM(NH) 1959.10.14.3 (Material of Williams, 1960: 708).
- [stomach] Plymouth, Devon, England (May, 1932) BM(NH) 1932. 1 1 .29.9 (Material of Baylis & Jones, 1933: 631); (Oct., 1972) BM(NH) 1983.11.7.13-14.
- [stomach] E of the Shetlands (60°N, 01°E; depth 116m; July, 1976). BM(NH) 1983.11.7.15.
- [stomach] Whiten Bank, N of Scotland (59°N, 05° W; depth 62-64 m; July, 1976) BM(NH) 1983.1 1.7.16; Pentland Firth (59°N, 02°W; depth 68 m; May, 1984) BM(NH) 1984.7.20.69.
- [stomach] Off St. Kilda. Collected by Z. Kabata. BM(NH) 1963.6.21.39^3.
[stomach] Hinkley, River Severn, England (Oct., 1973). Collected by D. C. Gardner. BM(NH)
1977.2.10.1.
- [stomach] Kristineberg, Sweden (Aug., 1976). BM(NH) 1983.11.7.17.
[?] Buchan Deeps, E of Scotland (Feb., 1963). Collected by K. MacKenzie. BM(NH) 1983.1 1.7.18.
Merluccius merlucdus [stomach] Plymouth, Devon, England (Oct., 1972). BM(NH) 1983.1 1.7.19. Molva molva [stomach] Plymouth, Devon, England. Collected by M. Rothschild, BM(NH) 1932.11.22.52; (May, 1932) BM(NH) 1932.1 1.28.50-54 (Material of Baylis & Jones, 1933: 631).
- [stomach] Kristineberg, Sweden (Aug., 1976). BM(NH) 1983.11.7.20-33.
- [stomach] NE of Scotland (57°N, 01°W; depth 67m; June, 1982). BM(NH) 1983.11.7.34. Myoxocephalus scorpius [stomach] Aberdeen, Scotland (Oct., 1973). BM(NH) 1983.11.7.35.
Pagellus bogareveo [stomach] Plymouth, Devon, England (May, 1972). BM(NH) 1983.11.7.36-37; (Oct.,
1972) BM(NH) 1983.11.7.38. Phycis blennoides [stomach] WSW of Barra Head, Scotland (57°N, 09°W; depth 656-665 m; April, 1973).
BM(NH) 1983.1 1.7.39. Platichthys flesus [stomach] Aberdeen, Scotland. (March, 1969) BM(NH) 1983.11.7.40; (Oct., 1973)
BM(NH) 1983.1 1.7.41. - [stomach] Ythan estuary, Aberdeenshire, Scotland (all year round). BM(NH) 1983.11.7.42-56
(Material of Gibson, 1971).
- [stomach] Plymouth, Devon, England. BM(NH) 1972.3.27.8; (May, 1972) BM(NH) 1983.11.9.1. [stomach] Loch Ewe, Scotland. BM(NH) 1983.11.9.2.
Pollachius pollachius [stomach] Northern North Sea. (59°N, 02°E; depth 98 m; May, 1983) BM(NH)
1983.11.9.3; (59°N, 06°W; depth 84m; May, 1984) BM(NH) 1984.7.20.65. Pollachius virens [stomach] Aberdeen, Scotland (Oct., 1973). BM(NH) 1983.11.9.4-^0.
- [stomach] Ythan estuary, Aberdeenshire, Scotland. BM(NH) 1972.3.27.10.
- [stomach] St. Andrews, Scotland. Collected by D. R. R. Burt. BM(NH) 1983.1 1.9.41.
- [stomach] NW of Flannan Isles, Scotland (59°N, 08°W; depth 144m; July, 1976). BM(NH) 1983.11.9.42.
- [stomach] Whitby, Yorkshire, England (Jan., 1974). Collected by G. Boxshall. BM(NH) 1976.1.5.62-100.
[stomach] 'Dog Hole', off NE Scotland (578N, J02°W; depth 75m; May, 1983). BM(NH)
1983.6.21.4-13 and 1983.11.9.43. Salmo trutta [stomach] Kristineberg, Sweden (Aug., 1976). BM(NH) 1983.1 1.9.44-63.
- [?] Off Ringsend, Co. Dublin, Eire (July, 1978). Collected by E. Fahy. BM(NH) 1978.12.6.1-50 and
1979.3.1.11. Scophthalmus rhombus [stomach] Aberdeen, Scotland (Oct., 1973). BM(NH) 1983.1 1.9.64-66.
HEMIURIDAE 1 5
Taurulus bubalis [stomach] Kristineberg, Sweden (Aug., 1976). BM(NH) 1983.1 1.9.67-68.
- [stomach] Wembury, Plymouth, Devon, England (Oct., 1980). BM(NH) 1983.11.9.69.
Trachurus trachurus [?] Firth of Forth, Scotland (Aug., 1963). Collected by K. Mackenzie. BM(NH)
1983.11.9.70. Trigloporus lastoviza [stomach] Plymouth, Devon, England (May, 1932). BM(NH) 1932.1 1.29.10 (Material
of Baylis & Jones, 1933: 631).
Trisopterus luscus [stomach] Plymouth, Devon, England (Oct., 1980). BM(NH) 1983.11.9.71-72. Trisopterus minutus [stomach] Off St. Kilda. Collected by Z. Kabata. BM(NH) 1963.6.21.39-43.
- [stomach] Kristineberg, Sweden (Aug., 1976). BM(NH) 1983.11.9.73-82.
- [stomach] Off North Rona, Scotland (59°N, 06°W; depth 84m; May, 1984). BM(NH) 1984.7.20.66. Zoarces viviparus [stomach] Firth of Forth, Scotland (July, 1963). Collected by K. MacKenzie, BM(NH)
1983.11.9.83.
(b) From elsewhere None.
(ii) NE Atlantic records from the literature
Most of the 19th century records of Distoma(-um) and Apoblema appendiculata are listed here, as H. communis is the commonest species of the genus in the NE Atlantic region. Some of these records could, however, have been other species of the genus or even species of other genera. (?) Acipenser sturio* [stomach] Ireland. Bellingham (1844: 425; as Distoma appendiculatuni). (?) Ammodytes tobianus [stomach] Ireland. Bellingham (1844: 425; as Distoma appendiculatuni). Ammodytes tobianus [stomach] Varberg, Sweden (July, Aug.). Olsson (1868: 49, fig. 98; as Distoma ocreatum Molin: see Odhner, 1905: 352, footnote).
— [oesophagus, stomach, intestine] St. Andrews, Scotland. Nicoll (1907: 71, 86).
— [intestine] Northumberland coast, England (June). Lebour (1908: 56).
(?) Anguilla anguilla [stomach] St. Andrews, Scotland. Nicoll (1907: 72; as H. appendiculatus). Anguilla anguilla [stomach] St. Andrews, Scotland. Nicoll (1909: 6, 20).
— [stomach] Bergen, Norway (Sept.). Olsson (1868: 46; as Distoma appendiculatuni: see Odhner, 1905: 351).
Argentina sphyraena [?] British coast. Halliday, in Scott (1969: 882).
Aspitrigla cuculus [?] Plymouth, Devon, England. Nicoll (1914: 484).
Blennius pholis [stomach] Widemouth, Bude, Cornwall, England (July). Matthews (19826: 152).
(?) Brosme brosme [?] Bergen, Norway (Aug.). Lonnberg (1890: 42; as Distoma appendiculatuni).
Brosme brosme [stomach] Aberdeen, Scotland. Nicoll (1913: 190).
Capros aper [?] Plymouth, Devon, England. Nicoll (1914: 484).
Ciliata mustela [stomach] Kristineberg, Sweden (Aug., 1903). Dollfus (19606: 705). Material of, but not
mentioned by, Odhner (1905:351). [stomach] Mumbles Head, Swansea, Wales. Srivastava (1966: 472).
— [stomach, intestine] Widemouth, Bude, Cornwall, England (July, Aug.). Matthews (19826: 161). Conger conger [stomach] Plymouth, Devon, England. Baylis & Jones (1933: 631); Baylis (1939: 477).
— [oesophagus, stomach, intestine] Roscoff, Finistere, France (June, 1937). Sproston (1939: 45, 50).
— [stomach] St. Andrews, Scotland. Gordon, in Laverack & Blackler (1974: 35).
Coregonus lavaretus oxyrinchus [stomach, caeca] Varberg, Sweden (Aug.). Olsson (1868: 46; as Distoma
appendiculatum: see Odhner, 1905: 351). (?) Dicentrarchus labrax [?intestine] (Rennes), Brittany, France. Dujardin (1845: 420; as Distoma (Apoblema)
appendiculatuni).
Entelurus aequoreus [?] Plymouth, Devon, England. Nicoll (1914: 484); Dawes (1947: 279). Eutrigla gurnardus [stomach] St. Andrews, Scotland. Nicoll (1909: 4, 20).
- [?] Plymouth, Devon, England. Nicoll (1914: 484).
— [intestine, stomach] North Sea, near Shetland Isles. Duniec (1980: 67; as H. luehei).
Gadus morhua [stomach] Varberg, Sweden; Alesund & Bergen, Norway (June-Sept.). Olsson (1868, 46; as Distoma appendiculatum: see Odhner, 1905: 351).
(?) [?] Kristineberg, Sweden (Aug.). Lonnberg (1889: 58; as Distomum appendiculatuni).
(?) [?] Bergen, Norway (July-Aug.). Lonnberg (1890: 40, 42; as Distomum appendiculatum).
*A very doubtful record. Other records from this host suggest that it might have been a lecithochiriine.
16 D. I. GIBSON & R. A. BRAY
- [stomach] Kristineberg, Sweden. Retzius (1909: 71); (July, 1898) Dollfus (1953: 78); (Aug., 1901) Dollfus (1953: 78); (Aug., 1903) Looss (1908: 106); Dollfus (19606: 705). All material of, but not recorded by, Odhner( 1905: 351).
- [stomach] St. Andrews, Scotland. Nicoll (1909: 5, 20); Gordon, in Laverack & Bladder (1974: 35).
- [stomach] Millport, Firth of Clyde, Scotland. Nicoll (1910: 350).
- [stomach] Galway, Eire. Little (1929: 25).
- [stomach] W of Scotland (July, 1954). Williams (1960: 708).
— [stomach] West coast of Norway. Meskal (1967: 13).
- [stomach] Scottish waters. Williams, McVicar & Ralph (1970: 48).
— [stomach] Havstensfjord & Gulmarsfjord (Kristineberg), Sweden. Thulin (1971: 78). 6resund, Sweden. Thulin( 198 1:22).
- [stomach] Bergen fish market, Norway. Kryvi (1972: 243; 1973: 273).
- [stomach] Kiel-Fjord, N Germany. Moller (1975o: 75; 19756: 8). [?] Western Kattegat to Bornholm in the Baltic. K0ie (1981: 61).
Gaidropsarus mediterraneus [stomach] Widemouth, Bude, Cornwall, England (May). Matthews (19826:
155).
(?) Gasterosteus aculeatus [stomach] Ostend, Belgium, van Beneden (1871: 40; as Distoma appendiculatd). (?) [?] Kristineberg, Sweden (July). Lonnberg (1889: 54; as Distomum appendiculatum).
— [stomach] Kristineberg, Sweden (Aug., 1901). Dollfus (19606: 705). Material of, but not mentioned by, Odhner( 1905: 351).
Gobius niger [stomach] Kristineberg, Sweden (Aug., 1901). Dollfus (19606: 705). Material of, but not
mentioned by, Odhner (1905: 351).
Gobius paganellus [?] Plymouth, Devon, England. Nicoll (1914: 484). Hippoglossoides platessoides [stomach] Bergen, Norway (July). Olsson (1868: 46; as Distoma appendiculatum;
see Odhner, 1905; 351).
- [stomach] Millport, Firth of Clyde, Scotland. Nicoll (1910: 350, 357).
Hippoglossus hippoglossus [stomach] Bergen, Norway (Aug.). Olsson (1868: 46; as Distoma appendiculatum; see Odhner, 1905:351).
— [stomach] St. Andrews, Scotland. Nicoll (1907: 72; as Hemiurus appendiculatus; 1909: 5, 20).
- [?] Trondheim, Norway (Sept., 1905). Dollfus (19606: 705).
- [stomach] W of Scotland (July, 1954). Williams (1960: 708). Hyperoplus lanceolatus [?] Plymouth, Devon, England. Nicoll (1914: 484).
Labrus bergylta [stomach] Millport, Firth of Clyde, Scotland. Nicoll (1910: 350, 356). (?) Lampetrafluviatilis [intestine] Belgian coast, van Beneden (1871: 90; as Distoma appendiculatd). Lepadogaster lepadogaster [?] Plymouth, Devon, England. Nicoll (1914: 484).
(?) Limanda limanda [?] New Brighton, Cheshire, England. Johnstone (1906: [174] 318; as Distomum appendiculatum).
- [stomach] Aberdeen, Scotland. Nicoll (1913:190).
— [?] Western Kattegat and 0resund. K0ie (1981: 61); [stomach] 0resund, Kattegat, off west Jutland (depth 10-32 m). K0ie (1983: 204).
Liparis montagui [?] Northumberland, England. Crofton (1947: 62).
Lophius piscatorius [stomach] Plymouth, Devon, England. Nicoll (1914: 484); Baylis & Jones (1933: 631); Baylis (1939: 477); Dawes (1947: 279); Matthews (19826: 151).
— [?] NE Atlantic. Gaevskaja (1978a: 83; possibly not an original record).
(?) Melanogrammus aeglefinus [mouth, stomach, caeca, intestine] Belgian coast, van Beneden (1871: 57; as Distoma appendiculatd).
- [stomach] St. Andrews, Scotland. Nicoll (1907: 71, 86).
Merlangius merlangus [buccal cavity] Bergen, Norway (Aug.). Olsson (1868: 46; as Distoma appendiculatum; see Odhner, 1905:351).
- [stomach] Kristineberg, Sweden (Aug., 1901). Dollfus (19606: 705). Material of, but not recorded by, Odhner (1905: 351).
— [stomach] Shoals, Irish Sea (March, 1906). Johnstone (1907: 280; as Distomum appendiculatum).
— [stomach] Northumberland coast, England. Lebour (1908: 56).
- [stomach] Plymouth, Devon, England. Nicoll (1914: 484); Baylis & Jones (1933: 631); Baylis (1939: 477); Dawes (1947: 279).
- [stomach] Galway, Eire. Little (1929: 25).
- [stomach] W of Scotland (July, 1954). Williams (1960: 708).
[stomach] Isle of Man, Irish Sea. Shotter (1969: 15; 1970: 36; 1972: 121; 1973a: 189; 19736: 563; 1976:
103). Some of this material is probably H. luehei.
HEMIURIDAE 17
Micromesistius poutassou [stomach] Off Rockall (Nov., 1975). Mackenzie (1979: 10). Molva molva [stomach] Bergen, Norway (Aug.). Olsson (1868: 46; as Distoma appendiculatum; see Odhner, 1905: 351).
- [stomach] Plymouth, Devon, England. Nicoll (1914: 484); Baylis & Jones (1933: 631); Baylis (1939: 477).
Myoxocephalus scorpius [stomach] Kristineberg, Sweden (Aug., 1901). Dollfus (19606: 705). Material of, but not recorded by, Odhner (1905: 351).
— [stomach] Bergen, Norway (Sept.). Olsson (1868: 46; as Distoma appendiculatum; see Odhner, 1905: 351).
- [intestine] Northumberland coast, England. Lebour (1908: 56); Crofton (1947: 62). [stomach] Plymouth, Devon, England. Baylis & Jones (1933: 631); Baylis (1939: 477).
Pagellus bogaraveo [stomach] Aberdeen, Scotland. Nicoll (1913: 189).
- [?] Plymouth, Devon, England. Nicoll (1912: 200; 1914: 484).
- [stomach] Galway, Eire. Little (1929: 26).
Pholis gunnellus [intestine] St. Andrews, Scotland. Nicoll (1907:71; as Hemiurus appendiculatus; 1909:
5, 20).
Platichthys flesus [stomach] Galway, Eire. Little (1929: 26). (?) [?] Walney Channel, Barrow-in-Furness, Cumbria, England. Markowski (1966: 192; specimens in
BM(NH) collection are Brachyphallus crenatus). [stomach] Ythan estuary, Aberdeenshire; off Aberdeen; Loch Ewe, Scotland. MacKenzie & Gibson
(1970: 4). Ythan estuary and Dee estuary, Aberdeenshire; sea off Aberdeen, Scotland. Gibson (1972: 6). [?] Kiel-Fjord, N Germany. Moller (1974: 138; 19756: 8).
(?) Pleuronectes platessa [?] New Brighton, Cheshire, England. Johnstone (1906: [174] 318; as Distomum appendiculatum).
- [stomach] Galway, Eire. Little (1929: 26).
- [stomach] Loch Ewe, NW Scotland. MacKenzie (1968: 15); MacKenzie & Gibson (1970: 4).
- [?] (Fish farm) Ardtoe, Argyle, Scotland. DAFS (1972a: 42).
- [?] (Fish farm) Hunterston, Ayrshire, Scotland. DAFS (19726: 35).
[?] (Fish farm) Moidart, Inverness-shire, Scotland. MacKenzie et al. (1976: 4).
Pollachius pollachius [stomach] Bergen, Norway. (Aug.) Olsson (1868: 46; as Distoma appendiculatum; see
Odhner: 1905, 351). (July) Lonnberg (1890: 42; as Distomum appendiculatum).
— [?] Kristineberg, Sweden. Juel (1889: 4; as Apoblema appendiculatum; see Odhner, 1905: 351). (July)
Lonnberg (1889: 58; as Distomum appendiculatum).
- [stomach] Millport, Firth of Clyde, Scotland. Nicoll (1910: 357).
- [stomach] Aberdeen, Scotland. Nicoll (1913: 189).
- [?] Plymouth, Devon, England. Nicoll (1914: 484).
- [stomach] Galway, Eire. Little (1929: 25).
[stomach] W of Scotland (July, 1954). Williams (1960: 708).
[stomach] Isle of Man, Irish Sea. Cubbin (1969: 52).
Pollachius virens [stomach] Bergen, Norway. (Sept.) Olsson (1868: 46; as Distoma appendiculatum; see
Odhner, 1905: 351); (July) Lonnberg (1890: 42; as Distomum appendiculatum). (?) [?] Kristineberg, Sweden (Aug.). Lonnberg (1889: 58; as Distomum appendiculatum).
- [stomach] Millport, Firth of Clyde, Scotland. Nicoll (1910: 350, 356). — [stomach] Loch Craiglin, Argyll, Scotland. Raymont (1952: 1 1 1).
- [stomach] Isle of Man, Irish Sea. Cubbin (1969: 51).
- [stomach] Bergen Fish Market, Norway. Kryvi (1972: 243; 1973: 273).
Raniceps raninus [stomach] Kristineberg, Sweden (Jan., 1903). Dollfus (19606: 705). Material of, but not
mentioned by, Odhner (1905: 351). Salmo salar [stomach] Varburg, Sweden (Aug.). Olsson (1968: 46; as Distoma appendiculatum; see Odhner,
1905: 351).
(?) [stomach] Bahusiae (? Bohuslan), Sweden (Aug.). Olsson (1876: 20; as Distoma appendiculatum).
(?) [stomach] Sundsvall, Sweden (July). Olsson (1893: 12; as Distoma appendiculatum}.
- [?] River Exe, Devon, England. Kennedy (1975: 66).
Salmo trutta [stomach] Bergen, Norway (Sept.). Olsson (1868: 46; as Distoma appendiculatum; see Odhner,
1905: 351). (?) [?] Kristineberg, Sweden (June). Lonnberg (1889: 58; as Distomum appendiculatum).
- [stomach] Kristineberg, Sweden (Aug., 1902). Dollfus (19606: 705). Material of, but not mentioned by, Odhner (1905: 351).
[?] t'Horntje, Texel, Netherlands. Willemse (1968: 84).
18 D. I. GIBSON & R. A. BRAY
Scophthalmus rhombus [stomach] Bergen, Norway (Aug.). Olsson (1868: 46; as Distoma appendiculatum; see
Odhner, 1905: 351).
Sebastes marinus [stomach] East coast of Iceland (67°N, 12°W; depth 105 m; Aug., 1948). Rees (1953: 20). Solea solea [stomach] Whitstable, Kent, England. El Maghraby & Perkins (1956: 486). (?) Taurulus bubalis [?] Kristineberg, Sweden (July). Lonnberg (1889: 54; as Distomum appendiculatum). [stomach] Kristineberg, Sweden (Sept., 1903). Dollfus (19606: 705). Material of, but not mentioned by,
Odhner (1905: 351).
— [stomach] St. Andrews, Scotland. Nicoll (1907: 70; as Hemiurus appendiculatus; 1909: 4, 20).
- [?] Plymouth, Devon, England. Nicoll (1914: 484).
- [stomach] Roscoff, Finistere, France (June, 1937). Sproston (1939: 50).
- [?] Northumberland coast, England. Crofton (1947: 62). [stomach] Widemouth, Bude, Cornwall. Matthews (19826: 158).
(?) Torpedo marmorata [stomach, intestine] Blankenberg, Belgium, van Beneden (1871: 16; as Distoma
appendiculatd).
Trachinus draco [stomach] Aberdeen, Scotland. Nicoll (1913: 189). Trachurus trachurus [?] ?NE Atlantic. Gaevskaja & Kovaleva (1980a: 53; 1982: 61).
- [?] English Channel. Gaevskaja & Kovaleva (19806: 19).
(?) Trigla lucerna [stomach, intestine] Belgian coast, van Beneden (1871: 30; as Distoma appendiculatd).
- [stomach] Galway, Eire. Little (1929: 25).
— [oesophagus] Roscoff, Finistere, France. Sproston (1939: 42).
Trigloporus lastoviza [stomach] Plymouth, Devon, England. Baylis & Jones (1933: 631); Baylis (1939: 477).
Trisopterus esmarkii [stomach] Faroes. Kabata, in Raitt (1968: 3-5).
Trisopterus luscus [?] Plymouth, Devon, England. Nicoll (1914: 484); Dawes (1947: 279).
- [stomach] Galway, Eire. Little (1929: 25).
- [gills] Roscoff, Finistere, France. Sproston (1939: 41, 50).
— [stomach] St. Andrews, Scotland. Gordon, in Laverack & Blackler (1974: 35).
[?] Ria de Muros-Noya, NW Spain. Martinez Fernandez, in Cordero del Campillo et al. (1975: 84).
Trisopterus minutes [stomach] Bergen, Norway (Aug.). Olsson (1868: 46; as Distoma appendiculatum; see
Odhner, 1905: 351). (?) [stomach] Bahusiae (? Bohuslan), Sweden (July, Aug.). Olsson ( 1 876: 20; as Distoma appendiculatum;
see Odhner, 1905:351).
- [stomach] Millport, Firth of Clyde, Scotland. Nicoll (1910: 350, 356).
- [?] Plymouth, Devon, England. Nicoll (1914: 484). Zeugopterus punctatus [?] Plymouth, Devon, England. Nicoll (1914: 484).
ASPECTS OF BIOLOGY. The full life-history of this species is not known, as information on the molluscan host and intra-molluscan stages is lacking. Presumably, the life-history follows a simi- lar course to that believed to occur in other hemiurids, i.e. egg, miracidium/mother sporocyst, redia, cystophorus cercaria. Dollfus (1923) has suggested that Cercaria calliostomae Dollfus, 1923, from the prosobranch Calliostoma zizyphinum might be the 'larval' form of a species of Hemiurus, and, if so, it is clear that H. communis is by far the commonest species of Hemiurus in the region of Roscoff, Brittany, where Dollfus' material came from, and indeed around Plymouth, where this cercaria has been recorded by Matthews (\982a, b). Unfortunately, it appears that the molluscan host Calliostoma zizyphinum has a Lusitanean distribution which is much wider than that of H. communis. The metacercariae of this species have been recorded on several occasions in the north-east Atlantic region from copepods, such as Acartia, from chaetognaths, especially Sagitta spp. and ctenophores (see pp. 5) by authors such as Lebour (1923, 1935) and Meek (1928). It is not known whether chaetognaths and ctenophores acquire their infestations directly or by feeding upon infested copepods. Small fish and fish-fry must, however, acquire the parasite directly from copepods and other planktonic invertebrates, but the majority of the larger fish presumably become infested by feeding upon small plankton-feeders, such as sand-eels, and other smaller infested teleosfts.
This parasite occurs in a wide variety of teleosts in British waters, but is especially common in gadoids. As discussed below, it is noticeably absent from pelagic, filter-feeding clupeids which harbour other species of the genus. As indicated by Gibson & Valtonen (1981) and Gibson (1982, 1983), H. communis has a distinctly boreal distribution (see below). Gibson (1972), studying this
HEMIURIDAE 19
20
15
J FMAMJJ AS ONDJ
MONTHS
Fig. 2 Hemiurus communis. Seasonal prevalence in Platichthys flesus from the estuary of the
River Ythan.
parasite in the flounder Platichthys flesus from two Scottish estuaries and from the sea nearby off Aberdeen, found it to be of little use as a biological tag.
Meskal (1967) deduced that the period of recruitment of young specimens of H. communis in the cod Gadus morhua off Norway commences in September, is at a maximum in November, and continues during the late autumn, winter and spring. He suggested that the old specimens die off between the summer and the following February. The life-span of this parasite in the cod appears, therefore, to be about eight months on average with a maximum of about 1 5 months. Gibson (1971), working with large numbers of flounders Platichthys flesus from the Ythan estuary, Aberdeenshire, found an autumnal peak in the prevalence of this parasite (Fig. 2). This peak is probably caused by flounders feeding upon small, infested saithe Pollachius virens and other small fishes which come inshore and often enter the estuaries at this time of the year, and by the addition of 0-group (recently metamorphosed) flounders to the population. These young fish presumably become infested by feeding directly upon planktonic invertebrates. Meskal (1967) noted a spring peak as well as an autumn peak in the prevalence of this parasite in cod. The absence of a spring peak in flounders can probably be explained by the fact that in spring, when normal feeding resumes after the winter reduction, many of the small teleosts which were eaten during the previous autumn are now too fast and too large to be eaten by flounders. In addition, many of the migratory forms, such as the saithe, will have moved back out to sea and away from the inshore and estuarine flounders.
Parasites with planktonic invertebrate hosts would be expected to infest most of the larger teleosts, firstly, when they are recently hatched and, secondly, when they are large enough to feed upon small, plankton-feeding fishes or smaller carnivorous forms. The results obtained by Gibson (1971) in flounders are presented in Fig. 3. These differ slightly from the expected results in relation to the younger fish, possibly because of the longevity of the parasite; those remaining from the 0-group infestation possibly obscuring a limited recruitment by 1 -group fish.
As mentioned above, it is clear from the records that H. communis appears to have a relatively restricted boreal distribution. Most of the records are on the continental shelf between Trondheim in Norway and Brittany in France, and the majority of these occur within the lati- tudes of Great Britain, extending eastwards into the Baltic Sea. The extreme limits of the records in our region range from a single specimen off Iceland mentioned by Rees (1953) to its presence in the Ria de Noya, NW Spain, reported by Fernandez, in Cordero de Campillo et al (1975). Outside our region, Polyanski (1955) indicated that it was rare in the Barents Sea, Pogorel'steva (1952) and Nikolaeva (1963) claim to have found it in the Black Sea, and Ronald (1960) lists it as occurring off the eastern coast of Canada. The isolation of the latter three records and the difficulties encountered in distinguishing this species from some other members of the family,
20
D. I. GIBSON & R. A. BRAY
7
/o
25 i
20
15
10
0+ 1+ 2+ 3* AGE-GROUP
4+
Fig. 3 Hemiurus communis. Prevalence in different age-groups of Platichthysflesus from the estuary of
the River Ythan.
especially poorly preserved material, indicate, in our opinion, that the presence of this species in the Black Sea and on the western side of the Atlantic Ocean requires confirmation. Appy & Burt (1982) stated that H. communis may 'be absent from the western Atlantic' and called for confirmation of reports to the contrary.
Kryvi (1972, 1973) studied the ultrastructure of the tegument and suckers of this parasite,
PREVIOUS DESCRIPTIONS. Odhner (1905: 351; brief, no figure); Nicoll (1907: 86; no figure); Lebour (1908: 56); Looss (1908: 106; brief, no figure); Raymont (1952: 114; some morphometric details); Dollfus (1953: 73; 1960: 704; figures of types); Srivastava (1966: 472; brief); Reimer (1970: 78; brief).
DESCRIPTION (Figs 4 & 5). The body of this worm is elongate and fusiform, its length depending greatly upon the extent to which the ecsoma is extruded. The latter structure may be completely withdrawn or extended until it occupies more than one-third of the total length of the worm. It is noticeable in small specimens that a double invagination of this organ often occurs (see Fig. 4B). The body-surface is covered with annular plications (Fig. 4F) ventrally and laterally, although they become less distinct in the posterior region of the body-proper (soma). In the larger speci- mens the dorsal plications occur only at the anterior extremity, extending posteriorly to the level of the pharynx or the intestinal bifurcation; but in smaller specimens the plications may occur, often very distinctly, back to the level of the seminal vesicle (Figs 4 & 5). Plications do not occur on the ecsoma, although under certain conditions, and especially in frozen material, the presence of circular muscles in the body-wall can give rise to small annular ridges, both on the ecsoma and on the rest of the body (Fig. 4E). In specimens which have been frozen or allowed to relax in tap- water prior to fixation the annular plications may*be lost. The oral sucker is ventrally subterminal and surmounted by a small pre-oral lobe. The ventral sucker, which is roughly one and a half to twice the size of the oral sucker (according to Raymont, 1952, this ratio increases slightly with the size of the worm), occurs well inside the anterior third of the soma. Measurements of this species are given in Table 2.
HEMIURIDAE
21
i
Fig. 4 Hemiurus communis. (A) Entire worm, ex Merlangius merlangus; (B) Entire worm, ex Limanda limanda; (C) Sagittal section of forebody, ex Scophthalmus rhombus; (D) Sagittal section of forebody, ex Pollachius virens; (E) Annulations on ecsomal surface of frozen specimen, ex Platichthys flesus; (F) Plications on surface of well-fixed specimen, ex Limanda limanda. Scale bars A,B 500 /mi; C,D 100/mi;E,F20/mi.
22
D. I. GIBSON & R. A. BRAY
Fig. 5 Hemiurus communis showing variations in morphology, laterality and postero-dorsal limit of plications (marked with lateral bars). (A) ex Gadus morhua; (B) ex Lophius piscatorius (flattened); (C) ex Salmo trutta; (D) ex Scophthalmus rhombus; (E) ex Pagellus bogareveo; (F) ex Conger conger; (G) ex Gadus morhua; (H) ex Cyclopterus lumpus; (I) ex Dicentrarchus labrax; (J) ex Trisopterus minutus. Scale bar: 500 fan.
There is no prepharynx. The muscular pharynx gives rise posteriorly to a very short oesophagus which extends posteriorly or dorsally, depending upon the state of contraction, to its union with the gut-caeca. The latter pass laterally and immediately dilate to form oval 'Driisenmagen', which possess an extremely deep, villous lining, Before passing posteriorly. They pass back down the body dorso-laterally and end blindly near the posterior extremity of the soma, or, when the ecsoma is extruded, they may extend some distance, sometimes deeply, into it.
The excretory pore opens terminally on the ecsoma. It leads into a tubular, Y-shaped excretory vesicle which bifurcates at about the level of the testes. The stem, which may initially wind in
HEMIURIDAE Table 2 Measurements of Hemiurus communis
23
|
Authority |
Nicoll (1907) |
Looss(1908) |
Dollfus (19606) |
Present material |
|
Host |
Ammodytes |
Gadus morhua |
Salmo trutta, |
Various hosts |
|
tobianus |
Myoxocephalus |
|||
|
scorpius, |
||||
|
Raniceps raninus |
||||
|
Locality |
St. Andrews, |
West Sweden |
Kristineberg, |
Various localities |
|
Scotland |
Sweden |
|||
|
Length (mm) |
1-5-2-5 |
2-0 |
1-8-3-53 |
0-45-4-0 |
|
Breadth (mm) |
0-42-0-57 |
0-4-0-45 |
0-43-0-78 |
0-105-0-85 |
|
Ecsoma (mm) |
<40% body length |
0-7 |
- |
0-1-5 |
|
Forebody (mm) |
- |
- |
- |
0-11-0-6 |
|
Oral sucker (mm) |
0- 11-0-1 8 diam. |
0-14 diam. |
0-1-0-15 x |
0-06-0-2 x |
|
0-12-0-19 |
0-05-0-22 |
|||
|
Ventral sucker |
0-1 6-0-26 diam. |
0-3 diam. |
0-19-0-31 diam. |
0-09-0-4 x |
|
(mm) |
0-08-0-4 |
|||
|
Sucker-ratio |
1 : 1-5-2-0 |
- |
- |
1:1-57-2-3 |
|
(usually 1:1-7- |
||||
|
1-9) |
||||
|
Testes (mm) |
0-1-0- 16 diam. |
- |
- |
0-02-0-22 x |
|
0-02-0-25 |
||||
|
Ovary (mm) |
0-1 1-0- 16x0-09 |
- |
- |
0-01-0-2 x |
|
0-02-0-22 |
||||
|
Vitelline |
- |
- |
- |
absent-0-3 x 0-32 |
|
masses (mm) |
||||
|
Eggs (/*m) |
22-31x9-13 |
19-21 x 10-12 |
21-24x9-12 |
22-29x9-15 |
|
(usually 24-28 x |
||||
|
10-12) |
specimens with withdrawn ecsoma, passes forward medially and slightly dorsally. The arms extend into the forebody ventro-laterally and unite dorsally to the pharynx.
The two oval testes occur obliquely in the anterior half of the hind body, usually about halfway between the ovary and the ventral sucker. One of the testes is normally situated slightly more dorsally than the other, but this can be either testis and either of them can be the more anterior. It is noticeable that the testes especially are variable in size, but all of the gonads tend to be smaller in relation to body-size in the larger specimens. The seminal vesicle consists of two globular or oval, contiguous lobes which are situated between the testes and the ventral sucker and close to the latter. The proximal lobe of this organ is normally the larger, although both are very variable in size, and may be larger than the testes. The proximal lobe usually has a slightly thicker and more muscular wall, but the thickness of the wall of both the portions varies considerably, depending presumably upon the volume of spermatozoa contained. Distally, the seminal vesicle gives rise to a tubular pars prostatica, which is lined with anuclear projections (blebs) that almost fill the lumen, surrounded by a dense, but narrow, covering of gland-cells and possesses a wall containing distinct longitudinal muscle-bundles. The pars prostatica passes anteriorly, dorsal to the ventral sucker, following an initially sinuous but then more direct course, to join the base of the sinus-sac. As it passes through the wall of the sinus-sac, the male duct loses its lining and external gland-cells and assumes the form of an undifferentiated ejaculatory duct. This very short duct unites with the metraterm to form an hermaphroditic duct just within the base of the sinus- sac (Fig. 4C, D). The sinus-sac is a tubular structure with a thick, muscular wall. It initially runs antero-ventrally in the middle of the forebody from a level just anterior to the ventral sucker, and then curves to run anteriorly to join a very short genital atrium. The median genital pore occurs
24 D. I. GIBSON & R. A. BRAY
close to the ventral margin of the oral sucker. The hermaphroditic duct, which extends through- out the length of the sinus-sac, has a wall which contains both longitudinal and circular muscles. The proximal (posterior) half of this duct is lined with what appears to be a villous coat, the 'villi' of which possess terminal and possibly detachable globules, somewhat similar to those described by Gibson (1976) in Paradinurus manteri Vigueras, 1958. The distal half of the duct is lined by a dense concentration of regular, papillate structures: this is, presumably, the region which is everted during copulation to form a temporary sinus-organ. There is no permanent sinus-organ. The subglobular ovary is situated close to the middle of the body, its position varying to some extent with the degree of contraction and/or the extent to which the ecsoma is extruded. It is normally separated from the testes by loops of the uterus. Details of the ovarian complex, which occurs postero-dorsally to the ovary, are difficult to make out, as it is very compact. The oviduct appears, however, to leave the ovary postero-dorsally, and, as it receives both the duct from JueFs organ and the common vitelline duct, it passes into a compact Mehlis' gland. The arrange- ment is, therefore, almost certainly very similar to that described below in detail for H. levinseni (see p. 30). .Fuel's organ is well developed, consisting of an oval 'inner vesicle', which contains active and disintegrating spermatozoa and an eosinophilic substance, and a surrounding amorphous mass, which contains a few, large, nucleate cells resembling amoebocytes. In some specimens the 'inner vesicle' of .Fuel's organ can be swollen with spermatozoa, giving the false impression that a small seminal receptacle is present (e.g. Dollfus, 1960&, fig. 1). In live specimens the 'inner vesicle' is very evident as a distinct, oval structure containing active spermatozoa. Egg-formation occurs in the proximal few narrow loops of the uterus, a region which we refer to as the uterine ootype (see Gibson & Bray, 1979). The next part of the uterus is wider and filled with spermatozoa, thus forming a distinct uterine seminal receptacle. The uterus then loops posteriorly, following a convoluted course, usually extending into the proximal region of the ecsoma when the latter is extruded. It then loops forward, filling much of the hindbody dorsally and also ventrally between the ovary and the testes and at the level of the seminal vesicle, before leading more directly forward dorsally to the ventral sucker. The uterus can pass the vitellarium on either the right or the left side of the body, but the dextral form seems to be slightly more common. In some specimens the distal extremity of the uterus, prior to its entry into the base of the sinus-sac, is constricted (Fig. 4C,D), forming a small vesicle which resembles that occurring in the genus Erilepturus Woolcock, 1935 ( = Uterovesiculurus Skrjabin & Guschanskaja, 1954). Within the sinus-sac the short metraterm unites with the ejaculatory duct to form the herma- phroditic duct. The uterus is normally filled with a great number of small, operculate eggs which lack spines or filaments. The vitellarium is composed of two large, symmetrical and oval or lobed masses, which occur immediately posterior to the ovary. In the larger specimens the vitelline masses are unlobed, but in the smaller worms the degree of lobation varies (Fig. 5). When present, the lobes occur as three on one mass and four on the other. It is interesting that the mass with three lobes appears to be associated with the side of the body on which the uterus passes the vitellarium, so that there are distinct sinistral and dextral forms of this species. The vitelline ducts unite to form a common duct before the latter joins the oviduct.
DISCUSSION. During the course of our study of this worm, it became clear that well-fixed specimens could usually be split into two morphological groups:
A. Specimens which: (1) were 0-5 to 4-0 mm, but rarely less than 1 mm, in length; (2) were less distinctly plicated, the plications reaching dorsally no further back than the level of the intestinal bifurcation; (3) possessed unlobed vitelline masses; and (4) tended to possess only single invaginations of the ecsoma (see Fig. 5).
B. Specimens which: (1) were 0-5 to 2-5 mm, but rarely greater than 2 mm, in length; (2) were distinctly plicated, the plications reaching back dorsally to a level between the middle of the ventral sucker and the testes; (3) possessed lobfcd vitelline masses; and (4) tended to possess double invaginations of the ecsoma (see Fig. 5).
There appear to be no host-differences, as we have specimens of both forms from cod and other gadoids, although the 'B'-form appears to be more prevalent in sand-eels and flatfishes. It is rather interesting that our specimens from the type-host and locality are the 'B'-form, while
HEMIURIDAE 25
Dollfus' (19606) figures of the syntypes are clearly form 'A'. It seems most likely that form 'B' is merely a younger condition of form 'A'. This is suggested by some of the features which dis- tinguish them, i.e. the posterior limit of the dorsal plications and the degree of lobation of the vitelline masses, which vary in the same manner, although to a lesser extent, in other species of the genus. It might seem, however, that there is more to distinguish these two forms than separates H. appendiculatus and H. luehei; but in the latter case there are distinct host-differences, and in the case of H. communis there are specimens which could be considered as intermediate between the two forms. In our view, therefore, there is not sufficient evidence to justify splitting the traditional concept of H. communis into two. It may be worthwhile to emphasize that some of the distinguishing features mentioned above are visible only in well-fixed material (our specimens were fixed without pressure in G.A.A. or Berland's fluid) which have been removed from freshly killed hosts.
One intriguing feature of this species is that, except for one immature specimen from Sprattus sprat tus recorded by Reimer (1970) in the Baltic Sea, H. communis does not appear to have been found in clupeids. Considering that H. appendiculatus occurs only in certain clupeids and that H. luehei is common in certain clupeids, this is surprising, especially as H . communis is so common in a wide range of marine teleosts, its metacercaria occurs in planktonic invertebrates (assuming the determinations of these larval forms in the literature is correct), and because clupeids are plankton-feeders. This phenomenon suggests that some sort of physiological or immunological host-specificity is involved, for, unless small plankton-feeding fish, such as sand-eels, are obli- gatory intermediate hosts, and this does seem unlikely, it is difficult to envisage how any ecological host-specificity might apply.
Hemiurus levinseni Odhner, 1905 (?) Fasciola serrulata Muller, 1780. (?) Hemiurus serrulatus (Muller) Dollfus, 1968. (?) Fasciola scabrum Muller, 1784. (?) Distoma scabrum (Muller) Zeder, 1803.
(?) Distoma (Echinostomd) scabrum (Muller) of Rudolphi (1819) in part. (?) Apoblema scabrum (Muller) Juel, 1889.
Distoma appendiculatum (Rudolphi) of Olsson (1868) in part and Levinsen (1881). Distomum ocreatum Molin of Linton (1900, 1901) in part. Hemiurus lintoni* Pratt, in Linton, 1901.
Hemiurus (Metahemiurus) levinseni (Odhner) Skrjabin & Guschanskaja, 1954. Metahemiurus levinseni (Odhner) Brinkmann, 1975. Hemiurus odhneri Yamaguti, 1934.
TYPE-HOST AND LOCALITY. Boreogadus saida, Franz- Joseph's Fjord, East Greenland. RECORDS
(i) Material studied
(a) From the NE Atlantic
Arctogadus sp. (? pearyi) [stomach] NE Greenland (Aug., 1931). Collected from preserved fish by J. Thulin.
BM(NH) 1983.1 1.15.1-2. Boreogadus saida [stomach] Claveringfjord, NE Greenland (Aug., 1931). Collected from preserved fish by
J. Thulin. BM(NH) 1983.11.15.3-5.
Gadus morhua [stomach] Troms0, Norway (June, 1980). BM(NH) 1980.6.20.42^3. Hippoglossus hippoglossus [stomach] Ingolfshofdi, South Iceland (Oct., 1966). Collected by B. Manger.
BM(NH) 1983. 11. 15.6-7. Merlangius merlangus [stomach] Off NE Scotland (60°N, 01°E; depth 116m; July, 1976). BM(NH)
1983.11.15.8-9. Merluccius merluccius [stomach] Thistle Field, northern North Sea (61°N, Ol£°E; depth 160 m; May, 1983).
BM(NH) 1983.1 1.15.10.
* Although this name, which was proposed by Pratt, in Linton (1901) for Linton's material referred to as 'Distomum ocreatum Molin', is older than H. levinseni, it has remained unused. For the sake of stability (Article 23b of the ICZN 1985), and because Linton's material was probably a mixture of//, levinseni and Brachyphallus crenatus (Rud., 1802), we have refrained from using it.
26 D. I. GIBSON & R. A. BRAY
Micromesistius poutassou [stomach] Thistle Platform, North Sea (61 °N, 01 °E; depth 168m; May, 1984).
BM(NH) 1984.7.20.62. Salmo salar [?] River North Esk, Angus, Scotland. Collected by J. W. Smith. BM(NH) 1967.10.2.20-22.
- [intestine] River Lee, Eire (March, 1967). Collected by M. Kane. BM(NH) 1968.4.16.2. Trisopterus esmarkii [stomach] Locality unknown, but probably off the Scottish coast. Collected by
Z. Kabata. BM(NH) 1983.11.15.11-13.
Trisopterus minutus [stomach] North Sea, E of the Shetlands (60°N, 00^°E; June, 1975). Collected by G. Kruse. BM(NH) 1981.4.21.1-2.
(b) From elsewhere
Alosa pseudoharengus [stomach] Passamaquoddy Bay, New Brunswick, Canada (Aug., 1982). BM(NH)
1982.9.28.62-71. Boreogadus saida [stomach] Grand Bank, W of Newfoundland (47°N, 52°W; depth 172m; July, 1975);
Grand Bank, NW of Newfoundland (49°N, 51°W; depth 188m; July, 1975); Hamilton Inlet Bank,
Labrador, Canada (54°N, 54°W; depth 188 and 192 m; July, 1975). BM(NH) 1977.2.17.1-12 (Material of
Bray, 1979: 421). Gadus morhua [stomach] Funk Island Bank, NW of Newfoundland (51°N, 52° W; depth 226 m; July, 1975);
Banquereau, W of Nova Scotia, Canada (44°N, 57°W; depth 76m; July, 1975); Banquereau, N of Nova
Scotia, Canada (45°N, 57°W; July, 1975). BM(NH) 1977.2.17.13-20 (Material of Bray, 1979: 421). Hemitripterus americanus [stomach] Sable Island Bank, off Nova Scotia, Canada (43°N, 61°W; depth 72 m;
July, 1975). BM(NH) 1977.2.17.21-24 (Material of Bray, 1979: 421).
— [stomach] Passamaquoddy Bay, New Brunswick, Canada (Aug., 1982). BM(NH) 1982.9.28.95-96. Hippoglossus hippoglossus [stomach] Hamilton Inlet Bank, off Labrador, Canada (54°N, 55°W; depth
176m; July, 1975). BM(NH) 1977.2.17.25 (Material of Bray, 1979: 421). Myoxocephalus octodecemspinosus [stomach] Sable Island Bank (43°N, 61°W; depth 72m; July, 1975).
BM(NH) 1977.2.17.26 (Material of Bray, 1979: 421).
Phycis chesteri [?] Scotian Shelf, Canada (Jan., 1979). Collected by J. S. Scott. BM(NH) 1983.1.21.3-6. Reinhardtius hippoglossoides [stomach] Hamilton Inlet Bank, W of Labrador, Canada (54°N, 54°W; depth
192m; July, 1975). BM(NH) 1977.2.17.27 (Material of Bray, 1979: 421). Urophycis chuss [stomach] Passamaquoddy Bay, New Brunswick, Canada (Aug., 1982). BM(NH)
1982.9.28.60-61.
(ii) NE Atlantic records from the literature
Boreogadus saida [stomach] Franz- Joseph's Fjord, East Greenland. Odhner (1905: 349). Eutrigla gurnardus [stomach, intestine] North Sea, near Shetland Isles. Duniec (1980: 67). Gadus morhua [stomach] W of Shetland Isles (Sept., 1954). Williams (1960: 708).
Micromesistius poutassou [intestine] Bergen, Norway (Aug.). Olsson (1868: 46; as Distoma appendiculatum; see Odhner (1905: 348).
- [?] Off Spitsbergen (77°N, 12°E) and/or Faroe Isles (62°N, 06°W). Szuks, Lorenz & Steding (1978: 144).
- [?] ?North Sea, Celtic Sea, SW Irish Sea ?or Bay of Biscay. Gaevskaja (19786: 4). Phycis blennoides [mouth] Skagen, Denmark. Odhner (1905: 349, footnote).
(?) Pollachius pollachius* [intestine] Ireland. Bellingham (1844: 427; as Distoma scabrum).
(?) * [intestine] Ostende, Belgium (June), van Beneden (1871: 61; as Distoma (Echinostomd) scabrd).
(?) Pollachius virens [stomach] Loch Craiglin, Argyllshire, Scotland. Raymont (1952: 116; as Hemiurus
communis).
Salmo salar [?] British Isles. Pippy (1980: 78).
(?) Trisopterus esmarkii [stomach] Faeroe Isles. Kabata, in Raitt (1968: 3, 5). (?) Trisopterus luscus (as Gadi barbati)** [stomach] Denmark (Nov.). Miiller (1780: 3; as Fasciola serrulata;
1784: 31; as F. scabrum).
*These records are very questionable as they lack descriptions and because Rudolph! (1819) appears to have possibly confused Fasciola serrulata ( = F. scabrum of Miiller) with the acanthpcolpid genus Stephanos tomum Looss, 1899. According to Looss (1899) and Odhner (1905: 65, footnote) this led to the inclusion of this species with the echinostomes.
**Earlier workers have listed the host of Mullet's record as being Gadus morhua, but according to our information Gadus barbatus is a synonym of Trisopterus luscus. This species is not, however, common in Danish waters, although its close relative T. esmarkii is, and the latter species is known to harbour H. levinseni. Fasciola serrulata and F. scabrum have been listed as possible synonyms of both Hemiurus sp. by Looss (1899) and H. communis by Odhner (1905) and as a definite record of//, communis by Dollfus (1968). However, the sucker-ratio in M tiller's (1780) figures and the identity of the host which we favour suggests to us that, although H. communis and Brachyphallus crenatus cannot be ruled out, this species is most likely a synonym of H. levinseni.
HEMIURIDAE 27
ASPECTS OF BIOLOGY. Little is known about the biology of this species, but it is assumed that it has a similar life-history to H. communis. Scott (1969) presumed the second intermediate hosts off the eastern Canadian coast to be Acartia and Sagitta, but so far only Sagitta elegans has actually been incriminated, both in the Gulf of St. Lawrence by Weinstein (1966, 1967, 1974) and in the White Sea by Kulachkova (\912a, b). Nevertheless, it is worth noting that Walter et al. (1979) have recorded Hemiums sp. (presumably H. levinseni) from the White Sea in Temora longicornis, Acartia longiremis and Pseudocalanus elongatus.
Although H. levinseni appears essentially to be a parasite of gadoids and to a lesser extent salmonids, it is clear that it must initially be acquired by plankton-feeding fishes (including juvenile predatory fishes) before being passed on to the larger predatory fishes. As in the case of H. communis (see above), this parasite does not appear to occur in clupeids in our region. The nature of this apparent host-specificity may, however, be different to that exhibited by H. communis, as H. levinseni is known to occur in the NW Atlantic in Clupea (Cooper, 1915; Miller, 1941; Gaevskaja & Umnova, 1977) and Alosa (Gaevskaja & Umnova, 1977; see also p. 26), and in the North Pacific in Clupea (Skrjabina, 1963; Arthur & Arai, 1980).
The paucity of our knowledge concerning this species prohibited Margolis (1963) from any definite conclusion on its value as a biological indicator of salmon in the northern North Pacific, and Scott (1969) showed that it was not suitable as an indicator for Argentina silas on the eastern coast of Canada. In his study of H. levinseni, Scott (1969) noted that 100 % prevalence occurred in young specimens of A. silas with an intensity of up to 200 per fish, falling to a low prevalence of about 15 % in mature fish with an intensity close to zero. Off the eastern Siberian coast Mamaev & Oshmarin (1963) reported that the prevalence in cod reached 92 % with an average intensity of 58, while it was totally absent in herring. They also stated that their results indicated that the parasite was acquired by fish in the sublittoral zone. In freshwater they found a prevalence of 4-7 % in Oncorhynchus nerka, and deduced that the range of this parasite in different species of salmon extended from the spawning ground in freshwater to the deep water of the northern Pacific Ocean. More recently, Appy & Burt (1982) found a prevalence of 89-7 % (up to 100 % in some regions) in cod in Canadian Atlantic waters.
H. levinseni appears essentially to be an arctic-boreal species (see Bray, 1979; Gibson & Valtonen, 1981; Gibson, 1982, 1983), probably having a circum-polar distribution which extends southerly into the northern North Atlantic and the northern North Pacific Oceans, especially, and to a greater extent, on the cooler western sides of these oceans. It occurs, therefore, only in the northern part of the area covered by this series, extending only as far south as the British Isles. As pointed out by Bray (1979) the record of this parasite from the Indian Ocean by Parukhin (1976a) w.ould appear to be very doubtful. It is worth noting that H. levinseni occupies a similar niche in arctic-boreal waters as does the hemiurid Elytrophalloides oatesi (Leiper & Atkinson, 1914) in antarctic-antiboreal waters.
PREVIOUS DESCRIPTIONS. Odhner (1905: 349); Looss (1908: 106); Cooper (1915: 188; encapsulated specimens); Manter (1926: 92); Yamaguti (1934: 432; as H. odhneri); Lloyd (1938: 115); Linton (1940: 123); Margolis (1956: 207; abnormal specimen); Zhukov (1960: 33); Hill (1974: 544); Grabda (1978: 21). (Many of these descriptions are brief.)
DESCRIPTION (Fig. 6). This small, spindle-shaped worm is relatively constant in shape, its ecsoma usually being either withdrawn or protruding only a short distance and rarely exceeding one quarter of the total body-length (Fig. 6). The body-surface, except for the ecsoma, is covered ventrally and laterally with annular plications, although these tend to fade out towards the pos- terior extremity. Dorsally the plications extend only as far back as the region between the ventral sucker and the ovary, but usually reach to the level of the testes. The oral sucker is ventrally subterminal, being surmounted by a small pre-oral lobe. The forebody is relatively long, usually being about one quarter of the total length of the soma, although it is sometimes less in con- tracted specimens. The ventral sucker, which is situated well inside the anterior half of the body, is similar in size to the oral sucker, the sucker-ratio (normally 1 : 0-9-1-1) not varying with body-size. Measurements of this species are given in Table 3.
28
D. I. GIBSON & R. A. BRAY
Fig. 6 Hemiurus levinseni. (A) Entire worm, ex Merlangius merlangus; (B) Entire worms, ex: (1) Gadus morhua, (2) Trisopterus esmarkii, (3) Hemitripterus americanus, (4) Salmo salar (flattened); (C) Sagittal section of forebody, ex Boreogadus saida; (D) Ovarian complex, ex Boreogadus saida: above, lateral view, below, exploded diagram. Scale bars: A 500 /mi; B 1 mm; C 200 /mi.
HEMIURIDAE
29
Table 3 Measurements of Hemiurus levinseni
|
Authority |
Odhner(1905) |
Manter(1926) |
Zhukov (1960) |
Present material |
|
Host |
Boreogadus saida |
Gadus morhua, |
Theragra |
Various hosts |
|
Urophycis chuss |
chalcogramma, |
|||
|
Onchorhynchus |
||||
|
gorbuscha |
||||
|
Locality |
Franz-Joseph's |
Maine, USA |
Sea of Japan, |
Various North |
|
Fjord, East |
Sea of Okhotsk |
Atlantic |
||
|
Greenland |
localities |
|||
|
Length (mm) |
1-1-6 |
0-99-1-68 |
1-3-4-16 |
0-79-2-9 |
|
Breadth (mm) |
1/3 length |
0-37-0-47 |
- |
0-17-0-55 |
|
Ecsoma (mm) |
withdrawn |
withdrawn |
- |
0-0-6 |
|
Forebody (mm) |
- |
- |
- |
0-19-0-63 |
|
Oral sucker (mm) |
0- 14-0-2 diam. |
0-14-0- 18 diam. |
- |
0- 1-0-23 x |
|
0-09-0-23 |
||||
|
Ventral sucker |
0- 11-0-1 7 diam. |
0-14-0- 19 diam. |
- |
0-08-0-22 x |
|
(mm) |
0-08-0-23 |
|||
|
Sucker-ratio |
Oral > ventral |
c. 1:1 |
- |
1:0-84-1-1 |
|
Testes (mm) |
- |
- |
- |
0-07-0-21 x |
|
0-06-0-25 |
||||
|
Ovary (mm) |
- |
- |
- |
0-08-0-23 x |
|
0-07-0-26 |
||||
|
Vitelline masses |
- |
- |
- |
0- 1-0-25 x |
|
(mm) |
0-07-0-23 |
|||
|
Eggs (/mi) |
26-28x12-13 |
23-26x10-13 |
25-29x12-13 |
20-27x10-15 |
|
(usually 23-26 x |
||||
|
10-13 |
There is no prepharynx, but the muscular, oval pharynx opens into a short, tegumental oesophagus which divides just posterior to the pharynx, giving rise to two dilate, lateral caeca which almost immediately open into the 'Driisenmagen'. These, in turn, open into the main part of the gut-caeca, which possess a glandular lining and extend back in the dorso-lateral fields. The rather wide caeca pass backwards, often sinuously, and terminate blindly either close to the base of the invaginated ecsoma or, when the latter is evaginated, often deep within it.
The excretory pore opens terminally on the ecsoma. It leads into a tubular, Y-shaped excretory vesicle which passes forward dorsally to the ovarian complex and bifurcates at a level between the anterior testis and the seminal vesicle. The arms pass forward laterally in the forebody and unite dorsally to the pharynx.
The two relatively large, globular or oval testes occur close together ventrally and obliquely, the dextral one being the more anterior, between the ovary and the ventral sucker and usually just anterior to the middle of the body. In relation to the size of the body, the testes are larger than in other species of the genus (in our specimens from salmon the testes are smaller than those in specimens recovered from other hosts; Fig. 6B4). The seminal vesicle consists of two oval lobes: these vary greatly in size, although the posterior (proximal) thin-walled lobe is usually the larger, sometimes exceeding the testes in size. The anterior (distal) lobe has a thicker wall, although it is not quite as thick as that of H . appendiculatus and H. luehei, and communicates with the pars prostatica via a short, aglandular duct (Fig. 6C). The tubular pars prostatica is much shorter than occurs in the latter two species and similar to that of H . communis. It winds between the seminal vesicle and the base of the sinus-sac, especially in the region immediately anterior to the seminal vesicle, passing dorsally to the ventral sucker. It is surrounded by a relatively dense con- centration of external gland-cells, which may be up to two cells in thickness (cf. H. appendiculatus), and to be lined by a layer of blebs (anuclear projections). At about the level of the anterior
30 D. I. GIBSON & R. A. BRAY
margin of the ventral sucker the pars prostatica passes, with the distal extremity of the uterus, through the wall of the proximal extremity of the sinus-sac. The ejaculatory duct is extremely short, as, once within the sinus-sac, the male and female ducts unite to form the hermaphroditic duct. The sinus-sac is tubular or slightly claviform, being slightly wider proximally. It lies medially, passing antero-ventrally and then curving to run anteriorly ventral to the pharynx before uniting with an extremely small genital atrium. This, in turn, opens to the exterior through the genital pore, which is situated mid-ventrally, close to the ventral margin of the oral sucker. As in the other species of the genus, the hermaphroditic duct appears to be divided into regions. The distal half is lined with a regular arrangement of small, tegumental knobs. This region is linked by a short, smooth region to the proximal half of the duct, which is lined by an irregular villous layer that appears to 'secrete' the extremities of the small 'villi' into the lumen (cf. the blebs lining the pars prostatica and also the ejaculatory vesicle of some lecithochiriines).
The large ovary is usually globular, but it is occasionally oval. It occurs close to the middle of the hindbody (excluding the ecsoma), being either contiguous with the posterior testis or, more often, separated from it by a small portion of the uterine coils. The remainder of the ovarian complex, present posterior or postero-dorsal to the ovary, is easier to decipher than in the other species of the genus. The oviduct passes posteriorly or postero-dorsally from the ovary and unites with the duct from Juel's organ, before curving ventrally to pass into Mehlis' gland. Immediately prior to its entry into this organ it receives the common vitelline duct. The part of the ovo- vitelline canal within Mehlis' gland can be referred to as the ootype, as the eggs do appear to be formed there. Having passed anteriorly or antero-dorsally it leaves Mehlis' gland and widens to become the uterus (Fig. 6D). The initial coils of the uterus dorsal and immediately posterior to Mehlis' gland contain spermatozoa in addition to eggs and, therefore, form a uterine seminal receptacle. Juel's organ (see Gibson & Bray, 1979) is large and surrounded by a distinct membrane. It occurs dorsally or antero-dorsally to the vitellarium and is often visible in whole- mounts (Fig. 6D). The 'inner vesicle' is somewhat tubular, being wide distally, but then narrow- ing proximally. It is irregularly convoluted within the organ and contains a loose concentration of what are presumably active spermatozoa which have recently passed through the ootype. The outer region of Juel's organ contains the usual amorphous material and quite a large number of cells which may be amoebocytes. The uterus winds posteriorly dorsal to the vitellarium until close to the base of the ecsoma, where it reflexes and loops forward ventrally, passing the vitellarium and the ovary on either the right or the left side of the body. Although forms with the uterus passing to the right of the vitellarium and the ovary (i.e. dextral forms) appear to be more common, the distribution of these forms in many cases does not appear to be random. All of our material from salmonids and the majority of our material from Merlangius, Hemitripterus and Boreogadus from the Hamilton Inlet Bank, Labrador, are sinistral, whereas the majority of our specimens from Gadus, Trisopterus and Boreogadus from off the Grand Banks, Newfoundland, are dextral. The uterus only occasionally extends into the ecsoma. Anterior to the ovary the uterus is quite wide. It passes forward to the right or the left side of the posterior testis in dextral and sinistral forms, respectively, although often partly overlapping it both ventrally and dorsally. It may or may not loop between the ovary and the posterior testis. After passing the anterior testis dorsally it usually loops ventrally or ventro-sinistrally to the pars prostatica, before narrowing and passing forward dorsally to the ventral sucker. At the level of the anterior margin of this sucker it enters the base of the sinus-sac, although often looping slightly into the forebody before doing so. The uterus contains numerous small, oval, operculate eggs which lack spines or filaments. The vitellarium is composed of two symmetrical, or occasionally slightly oblique, oval to globular masses which are present ventrally immediately posterior to the ovary. Even in the smallest specimens, there is little or no sign of any lobation on these masses.
DISCUSSION. Hemiurus levinseni can be readily (distinguished from the other species of the genus by sucker-ratio. Otherwise, it is morphologically somewhat similar to H. communis, although tending to have larger gonads and a less frequently evaginated ecsoma. It is also worth noting that even the smallest of our specimens were mature and gravid: this was not the case with the other species.
HEMIURIDAE 3 1
Skrjabin & Guschanskaja (1954) erected the subgenus Metahemiurus for H. levinseni, which they proposed as the type-species, and H. odhneri Yamaguti, 1934, because: (1) the oral sucker is larger than the ventral sucker; (2) the plications extend almost to the posterior end of the soma; and (3) the ecsoma is short. With a few exceptions (e.g. Slusarski, 1958; Brinkmann, 1975), the majority of workers have not accepted Metahemiurus as a valid taxon. Despite the fact that Brinkmann (1975) has used this name at the generic level, we cannot agree that there is any value in retaining this taxon, especially as we consider only some of the distinguishing criteria to be of value, and these only at the specific level. With regard to H. odhneri, we agree with Zhukov (1960) that this species falls within the morphometric range of H . levinseni and must, therefore, in the absence of other evidence, be considered a synonym.
Hcmiurus luehei Odhner, 1905*
(?) 'vermiculos' of Leeuwenhoek (1697).
(?) Fasciola halecis Gmelin, 1790 (Leeuwenhoek's 'vermiculos' named).
(?) Distoma halecis (Gmelin) Zeder, 1803.
(?) Hemiurus halecis (Gmelin) Dollfus, 1956.
Fasciola ocreata Rudolphi, 1802, nee Goeze, 1782 (nom. nov. pro Fasciola halecis Gmelin,).
Distoma ocreatum (Rudolphi) Rudolphi, 1809.
Distoma (Apoblema) ocreatum (Rudolphi) Dujardin, 1845.
Apoblema ocreatum (Rudolphi) Juel, 1889.
Pronopyge ocreata (Rudolphi) Looss, 1899.
Hemiurus ocreatus (Rudolphi) Odhner, 191 1.
Distoma appendiculatum (Rudolphi, 1802) of Olsson (1868) (in part).
(?) Distoma (Apoblema) appendiculatum (Rudolphi) of Dujardin (1845) (in part).
Hemiurus appendiculatus (Rudolphi) of Rioja (1923), (?) Dollfus (1929) and Patzelt (1930).
Distoma ventricosum Rudolphi, 1819 of Wagener (1860) (in part).
Hemiurus stossichi (Monticelli, 1891) of Liihe (190 la).
'Hemiurus stossichi Luhe, 1901' of Odening (1978).
Hemiurus rugosus Looss, 1907.
Hemiurus (Neohemiurus) raabei Slusarski, 1958.
Parahemiurus merus (Linton, 1910) of Rokicki (1973) and Gaevskaja (1977).
TYPE-HOST AND LOCALITY. Clupea harengus, Alesund, Norway. In the absence of a previously designated type-host and locality, we have used the first records given by Olsson (1868) on whose material Odhner (1905) erected this species.
RECORDS
(i) Material studied
(a) From the NE Atlantic
Brama brama [stomach] Buckie, Banff, Scotland (Oct., 1973). BM (NH) 1983.11.21.1.
Clupea harengus [stomach] Off NE Scotland (58°N, 02°W; depth 80 m; Dec., 1979). BM(NH) 1983.1 1.21.2.
- [?] Moray Firth (winter 1972-73). Collected by K. MacKenzie, BM(NH) 1983.11.21.3.
- [stomach] Turbot Bank, off NE Scotland (57°N, 01 °W; depth 67m; June, 1982). BM(NH) 1983.11.21.4.
Eutrigla gurnardus [?] Scotland, Collected by K. MacKenzie. BM(NH) 1983.11.21.5. Merlangius merlangus [intestine] Burnham-on-Crouch, Essex, England. BM(NH) 1962.11.1.1.
- [?] Port Erin, Isle of Man, Collected by R. A. Shotter. BM(NH) 1969.1.9.1. (Possibly part of material called//, communis by Shotter, 1969:15; 1970:36; 1972:121; 1973a: 189; 19736: 563; 1976: 103).
Platichthys flesus [stomach] Off Aberdeen, Scotland. BM(NH) 1972.3.27.11. (Material of Gibson, 1973: 463).
- [stomach] Ythan estuary, Aberdeenshire, Scotland (July, 1968). BM(NH) 1983.11.21.6.
Salmo salar [stomach] South of Dogger Bank, North Sea (55°N, 03°E). Collected by K. MacKenzie. BM(NH)1983.11.21.7^0.
'Originally referred to as H. Itihei, but the spelling of this name has since been amended in accordance with the Inter- national Code of Zoological Nomenclature.
32 D. I. GIBSON & R. A. BRAY
Salmo trutta [stomach] Kristineberg, Sweden (Aug., 1976). BM(NH) 1983.11.21.41-43.
Sordino pilchardus [stomach] Bay of Biscay (47°N, 02°W; Mar., 1980). BM(NH) 1983.1 1.21.44-45.
Scomber scombrus [stomach] St. Andrews, Scotland (July, 1949). Collected by D. R. R. Burt, BM(NH)
1983.12.14.11. Sprattus sprattus [stomach] Estuary of Riven Ythan, Aberdeenshire, Scotland. BM(NH) 1983.1 1.21.46.
- [stomach] Off Macduff, Banff, Scotland (58°N, 02°W; depth 100 m; May, 1984) BM(NH) 1984.7.20.61 .
(ii) From elsewhere
Clupea harengus membras [?] Baltic Sea (Apr., 1976). BM(NH) 1981.12.3.9. (Material of Gaevskaja, 1977:1 1: as Parahemiurus merus).
(b) NE Atlantic records from the literature
Capros aper [stomach] Plymouth, Devon, England. Nicoll (1914: 485; as Hemiurus ocreatus). (?) Clupea harengus [stomach] Netherlands (March). Leeuwenhoek (1697: 47; as 'vermiculos'; later named Fasciola halecis by Gmelin, 1790, and renamed Fasciola ocreata by Rudolphi, 1802).
- [stomach] B10den Ground, North Sea (1953). Hansen (1955: 62).
— [stomach] Alesund and Bergen, Norway (July, Aug.). Olsson (1868: 46; as Distoma appendiculatum; renamed H. liihei by Odhner, 1905: 351).
— [intestine] Belgian coast, van Beneden (1871: 66; as Distoma appendiculatd).
- [?] SE of West-Hinder (Dec., 1933); WNW of West-Hinder, 30 miles (48 km) from Ostende (Nov., 1933); 12 miles (19 km) W of West-Hinder (Dec., 1933). Markowski (1938: 6; as H. ocreatus).
— [stomach and caecum] St. Andrews, Scotland. Nicoll (1907: 72, 87).
- [stomach] Millport, Firth of Clyde, Scotland. Nicoll (1910: 350, 357).
- [?] Den Helder, Netherlands. Willemse (1968: 84; as H. ocreatus).
- [?] Northern North Sea. Reimer & Jessen (1972: 65).
- [?] Irish Sea (Sept.). Markowski (1938: 6; as H. ocreatus).
[?] Near Gravelines, Pas de Calais, France (Jan., 1934); between Gravelines and Calais, France, out-
side territorial waters (Dec., 1933 & Jan., 1934); Calais, France (Jan., 1933). Markowski (1938: 6; as H.
ocreatus).
Eutrigla gurnardus [stomach] St. Andrews, Scotland. Nicoll (1909: 4, 21). Gadus morhua [?] Western Kattegat to Bornholm in the Baltic. K0ie (1981: 61; as H. ocreatus). Merlangius merlangus [stomach] Plymouth, Devon, England. Nicoll (1914: 485; as H. ocreatus). Merluccius merluccius [stomach] Aberdeen, Scotland (Sept., 1908). Nicoll (1913: 189; as H. ocreatus).
— [stomach] Galway, Eire. Little (1929: 26; as H. ocreatus).
Platichthys flesus [stomach] Off Aberdeen, Scotland. Gibson (1973: 463; as H. ocreatus).
[?] Kiel Fjord region, North Germany. Moller (19756: 8; as H. ocreatus).
Pottachius pollachius [stomach] Plymouth, Devon, England. Nicoll (1914: 485; as H. ocreatus). (?) Salmo salar [gut] River Rhine at Basle, Switzerland.*
— [stomach] River Tweed, Great Britain. Tosh (1905: 116; as Distoma ocreatum). Salmo trutta [?] River Tweed, Great Britain. Tosh (1905: 1 16; as D. ocreatum).
Sardina pilchardus [stomach] Plymouth, Devon, England. Nicoll (1914: 485; as H. ocreatus}.
— [oesophagus] Marin, Pontevedra, Spain. Rioja (1923: 89; as H. appendiculatus). See also: Lopez-Neyra (1941: 332; 1947: 57).
[?] Muros-Noya, NW Spain. Martinez-Fernandez, in Cordero del Campillo et al. (1975: 84; as H.
ocreatus).
(?) Scomber scombrus [?intestine] Brittany (Rennes), France, Dujardin (1845: 420; as Distoma (Apoblema) appendiculatum).
— [stomach] Plymouth, Devon, England. Nicoll (1914: 485; as H. ocreatus).
— [stomach] St. Andrews, Scotland. Gordon, in Laverack & Blackler (1974: 35; as Pronopyge ocreata).
* Hemiurus luehei may have been recorded by Zschokke (1896: 776) and Hausmann (1897: 22) under the names Distomum ocreatum and/or Distomum appendiculatum; but Heitz (1918: 344) has listed these records as Brachyphallus crenatus (Rudolphi, 1802). As Heitz had fresh material and access to the literature of Odhner, Looss and Liihe, we have accepted his opinion. It is possible, however, that Zschokke (1890: J64; 1891: 697; 1896: 773) and Hausmann (1897: 4) recorded H. luehei under the name 'Distomum reflexum Creplin', for, although Zschokke's (1891) measurements are larger than those normally recorded for this species, his figure is somewhat similar if he confused the pars prostatica with the testes and the withdrawn ecsoma with the excretory vesicle. Earlier, van Beneden (1871) recorded '/). reflexum' from salmon, but his figure of this species from Cyclopterus lumpus appears to be rather similar to Derogenes varicus (Miiller). Distoma reflexum Creplin is in fact a species of the opecoelid genus Podocotyle Dujardin. '/). reflexum Creplin' of Zschokke was referred to as 'Distomum sp. nov.' by Liihe (1909).
HEMIURIDAE 33
Sprattus sprattus [stomach] Varberg, Sweden (July, Aug.). Olsson (1868: 46; as Distoma appendiculatum; renamed H. luheiby Odhner, 1905: 351).
— [stomach] Bergen, Norway (July, Aug.). Olsson (1868: 46; as Distoma appendiculatum; renamed H. liihei by Odhner, 1905:351).
(?) [caeca and intestine] Belgian coast, van Beneden (1871: 67; as Distoma appendiculatd).
— [stomach, caeca and intestines] St. Andrews, Scotland. Nicoll (1909: 4, 21).
- [?] North Sea (over wide area). Reimer (1978: 149).
Trachurus trachurus [stomach] Plymouth, Devon, England. Nicoll (1914: 485; as H. ocreatus).
- [?] English Channel. Gaevskaja & Kovaleva (19806: 19).
- [?] ?NE Atlantic. Gaevskaja & Kovaleva (1980a: 53; 1982: 61).
Trigloporus lastoviza [mouth] Roscoff, Brittany, France (June, 1937). Sproston (1939: 42, 55; as H. ocreatus).
ASPECTS OF BIOLOGY. Although Mobius, in Willemoes-Suhm (1871: 383) appears to have recorded ecsomate trematodes which he refers to as 'Distoma ocreatum Rud. der Haringe' from copepods in the Bay of Kiel, there seems to be no more certain record of the larval stages of this parasite. It is assumed, however, that it has a similar life-history to the other species of the genus, and that the metacercariae occur in planktonic invertebrates, such as copepods and chaetognaths. Hansen (1955) noted that 95 % of the diet of herring was crustaceans and most of these were calanoids. Thus the clupeid hosts presumably acquire the parasites directly; but it seems likely that the non-clupeids acquire the parasite, at least in part, by feeding upon clupeids or other plankton- feeders. We know this to be the case in flounders from the Ythan estuary, Aberdeenshire, which became infested by feeding upon sprats, and Tosh ( 1 905) noted that this parasite occurred in salmon and sea-trout, especially after they had been feeding upon herring. The apparent absence of this species from shad is difficult to explain, unless some sort of ecological or physiological specificity associated with their spawning migration into freshwater is involved, or unless immunological specificity occurs.
Little is known about the seasonal dynamics of this species, except that Hansen (1955) indicated that in North Sea herring prevalence is very low in winter, it increases in spring, is very high (about 70 % ) in summer and falls again during the autumn.
The distribution of H. luehei appears to mimic that of one of its major definitive hosts, Sprattus sprattus. The records extend between the latitudes of 35° and 65°N on the Atlantic coast of Europe and extend easterly into the Baltic, Mediterranean and Black Seas. There appears to be no definite record west of the continental shelf off Britain, thus, as mentioned by Gibson & Valtonen (1981) and Gibson (1982, 1983), this species of parasite has a Lusitanean distribution. As mentioned above, it may extend its range into freshwater in salmonids, and it has been recorded in carnivorous freshwater fishes, e.g. Reimer (1970) found it in Esox in the Baltic Sea and Borovitzkaya (1952) and Kulakovskaya & Koval (1973) have recorded it in Perca in the lower Danube.
Little else is known about H. luehei. It is worth noting that Gibson (1973) observed the presence of 'excretory corpuscles' in the excretory vesicle under the TEM.
PREVIOUS DESCRIPTIONS. Odhner (1905: 352); Nicoll (1907: 85); Looss (1908: 105; as H. liihei and H. rugosus); Rioja (1923: 89; as H. appendiculatus; see also Lopez-Neyra, 1941: 332; 1947: 57); Patzelt (1930: 6; as H. appendiculatus); Timon-David (1937: 17; as H. rugosus); Slusarski (1958: 384; as H. liihei and H. raabei); Reimer (1970: 76).
DESCRIPTION (Fig. 7). The body of this species is cylindrical, the posterior half usually being broader than the anterior half (Fig. 7). Even when the ecsoma, which can reach up to one third of the total body-length, is completely withdrawn, the body is still very elongate and cylindrical. The body-surface, except for the ecsoma, is covered ventrally and laterally with distinct annular plications. These tend to become less distinct towards the posterior end of the soma. Dorsally the plications tend to reach posteriorly as far as the level of the seminal vesicle or the testes. The oral sucker is ventrally subterminal and surmounted by a small pre-oral lobe. The ventral sucker, which is often directed antero-ventrally, is situated close to the oral sucker. It is about one and a
34
D. I. GIBSON & R. A. BRAY
Fig. 7 Hemiurus luehei. (A) Entire worm, ex Salmo trutta; (B) Flattened worm, ex Platichthys flesus; (C) Seminal vesicle; (D) Sagittal section of forebody, ex Salmo trutta. Scale bars: A 200 //m; B 500^m;C,D 100/^m.
HEMIURIDAE
35
Table 4 Measurements of Hemiurus luehei
|
Authority |
Nicoll (1907) |
Slusarski |
Reimer(1970) |
Present material |
|
(1958) |
||||
|
Name used |
H. liihei |
H. raabei |
H. luehei |
H. luehei |
|
Host |
Clupea harengus |
Salmo solar |
Clupea harengus, |
Various hosts |
|
Esox lucius |
||||
|
Locality |
St. Andrews, |
Baltic Sea |
Baltic Sea |
Various |
|
Scotland |
localities |
|||
|
Length (mm) |
2-7^-14 |
1-8-2-62 |
0-77-2-38 |
0-8-2-9 |
|
Breadth (mm) |
0-35-0-4 |
0-27-0-34 |
0-17-0-4 |
0-13-0-5 |
|
Ecsoma (mm) |
1/4-1/3 soma |
<l/3 soma |
- |
0-0-65 |
|
Ecsoma/body- |
20-25 |
«25) |
- |
0-31 |
|
length (%) |
||||
|
Forebody (mm) |
0-33-0-4* |
- |
- |
0-08-0-27 |
|
Oral sucker (mm) |
0- 11-0-1 3 diam. |
0-09-0-1 diam. |
0-38-0-1 Ix |
0-06-0- 13 x |
|
0-66-0-11 |
0-06-0-12 |
|||
|
Ventral sucker |
0-1 8-0-24 diam. |
0-15-0-16x |
0-1-0-2 x |
0-09-0- 19 x |
|
(mm) |
0-19-0-2 |
0-08-0-18 |
0-1-0-22 |
|
|
Sucker-ratio |
1:1-5-2 |
1:1-6-1-9 |
- |
1 : 1-43-2 |
|
(usually 1:1-5 |
||||
|
-1-8) |
||||
|
Seminal vesicle |
>25 |
- |
- |
13-28 |
to ventral sucker/body- length (%)
|
Testes (mm) |
0-1 4-0- 16 diam. |
0-03-0- 15 x |
0-06-0- 13 x |
|
0-05-0-19 |
0-05-0-18 |
||
|
Ovary (mm) |
0-13-0-18 x |
0-04-0- 16 diam. |
0-04-0- 13 x |
|
0-11-0-12 |
0-06-0-23 |
||
|
Vitelline masses |
similar to |
0-08-0-21 diam. |
0-05-0- 19 x |
|
(mm) |
ovary |
0-05-0-2 |
|
|
Eggs (//m) |
22-28x11-12 17-27x8-11 |
19-25x9-13 |
21-25x8-13 |
*Measurement from centre of sucker.
half to twice the size of the oral sucker, the ratio usually being about 1:1-5-1-8. The measurements of this species are given in Table 4.
There is no prepharynx, but the muscular, oval pharynx gives rise to a -short, oval oesophagus with a tegumental lining, which extends posteriorly and, in turn, give rise laterally to the gut- caeca. The latter bear 'Driisenmagen' in the 'shoulder'-region. The caeca then pass posteriorly, following a direct course in the dorso-lateral fields, and end blindly close to the posterior end of the body, normally within the ecsoma. The caeca usually extend only into the proximal half of the ecsoma when it is protruded, although normally further than the uterus; but occasionally they may almost reach the posterior end. When the ecsoma is withdrawn, the caeca may not enter it at all (Fig. 7A).
The excretory pore is terminal on the ecsoma. The excretory vesicle is Y-shaped, the narrow stem passing forward medially in the hindbody dorsal to the vitellarium and dividing in the ventral field at the level of the seminal vesicle. The two arms pass forward laterally into the forebody and unite dorsally to the pharynx.
The two oval testes occur in tandem or slightly obliquely just anterior to the middle of the hindbody (excluding the ecsoma) and slightly posterior to a point half-way between the ventral sucker and the ovary; but these arrangements are somewhat variable, depending upon the state of contraction. The seminal vesicle, which occurs immediately anterior to the testes, consists
36 D. I. GIBSON & R. A. BRAY
of two contiguous, oval lobes, the anterior of which possesses a thick, muscular wall and is occasionally without spermatozoa. This lobe, which is usually the smaller of the two, is usually tear-shaped, often with its tapering distal region constricted slightly by a sphincter muscle (Fig. 7C). In some cases, this constriction can give the impression that the seminal vesicle is trilobed. The tapering region of the anterior lobe leads directly into a very long, tubular pars prostatica. This duct, which is surrounded by a relatively dense, but single, layer of oval gland-cells and lined by a layer of anuclear blebs, passes forward in the ventral field following a convoluted or sinuous path, depending upon the state of contraction. After passing the ventral sucker dorsally it unites with the metraterm just inside the base of the sinus-sac at about the level of the anterior margin of this sucker (Fig. 7D). The ejaculatory duct, i.e. the region of the male duct within the sinus-sac, is very short. The sinus-sac is usually cylindrical, but sometimes the proximal third is slightly pinched off into a broad, oval region. It possesses a thick, muscular wall and extends anteriorly to unite with a very small genital atrium, which opens mid-ventrally through the genital pore medially and close to the ventral margin of the oral sucker. Within the sinus-sac the hermaphro- ditic duct can be seen to be divided into two distinct regions which are united by a short, undiffer- entiated region of the duct. The nature of the two regions of this duct is not absolutely clear in our sectioned specimen, which is small; but they appear to be similar to other species of the genus in that the proximal region appears to possess an irregular, villous lining and the distal region possesses a regular, papillate (knobbed), tegumental lining.
The transversely oval ovary is usually present about half-way between the testes and the posterior end of the soma and is separated from the testes by a large proportion of the uterine coils. Although its position is variable, depending upon the degree of contraction, unlike H. appendiculatus, it does not appear to enter the ecsoma. The remainder of the ovarian complex is compact and difficult to decipher, but a distinct Juel's organ with an oval 'inner vesicle' is visible. After receiving the duct from Juel's organ and the common vitelline duct proximally, the oviduct then passes through Mehlis' gland. The initial coils of the uterus, which lie dorsally to the vitellarium, contain spermatozoa, and thus form a uterine seminal receptacle. The uterus con- tinues posteriorly following a convoluted course usually into the proximal region of the ecsoma, although on rare occasions it can extend close to the posterior extremity and in some cases, when the ecsoma is withdrawn, it does not penetrate the ecsoma at all. The uterus then reflexes anteriorly, passing dorsally to the ovarian complex and following a convoluted course. The greatest region of uterine coils is between the ovary and the posterior testis, where they com- pletely fill the entire width of the worm. The uterus passes the testes, seminal vesicle and pars prostatica dorsally, being either coiled, sinuous or running forward relatively directly. In this region it becomes narrower and then passes forward to enter the base of the sinus-sac. A short distance prior to its entry into this organ, there are indications in some specimens of a constriction caused by a sphincter muscle. The uterus is filled with numerous small, operculate eggs which lack spines or filaments. The vitellarium is composed of two entire or slightly lobed masses which occur symmetrically and ventrally immediately posterior to the ovary. The lobes, which normally occur as three on one mass and four on the other, are more often seen in small specimens.
DISCUSSION. It seems likely that this species was first recorded by Leeuwenhoek (1697) in herring. Unfortunately, his description is not really adequate to indicate either the species or the genus, for, although it does seem likely that it was H. luehei, related forms, such as Br achy phallus crenatus (Rudolphi, 1802), have occasionally been recorded from herring in European waters. Leeuwenhoek's material was later named Fasciola halecis by Gmelin (1790), and this was again renamed Fasciola ocreata and redescribed from his own material by Rudolphi (1802). Unfortunately, the latter is a junior homonym of F. ocreata Goeze, 1 782, which is now the type-species of Ityogonimus Liihe, 1899. This homonymity was probably overlooked because F. ocreata of Goeze (1782) and F. ocreata of Rudolphi (1802) were quickly transferred to Monostoma and Distoma by Zeder (1800) and (1803), respectively. Although Odhner's (1911) examination of Rudolphi's material has shown conclusively that it is a Hemiurus, there was considerable confusion concerning this name during much of the latter half of the 19th century. As we have explained in our publication on the Fellodistomidae (Bray & Gibson, 1980), the
HEMIURIDAE 37
appellation Distoma (-urn) ocreata (-um) was used by several authors for the species which we now refer to as Pronoprymna ventricosa (Rudolphi, 1819). In addition, specimens of the present species were often referred to as Distoma appendiculatum. The first available name which we can be absolutely certain pertains to the species of Hemiurus which occurs commonly in the stomachs of herring, sprats and pilchards is H. luehei Odhner, 1905, and this is the name which we are accepting in this work. The majority of recent workers have used the name H. ocreatus (Rudolphi, 1802), since Odhner (1911) considered it a senior synonym of H. luehei; but the homonymity described above definitely precludes its usage (ICZN 1985, Article 57b). Dollfus (1956, 1968) has resurrected Gmelin's name and referred to this species as Hemiurus halecis; but, as mentioned above, we cannot be absolutely certain about the identity of Leeuwenhoek's material. Although the term 'nomen oblitum' has now been deleted from the ICZN, we feel that, as the name had remained unused since before 1830, except for two references to it as a junior synonym, it would, in any case, be unwise to resurrect it now.
Since Odhner's (1905) work, in which he listed Hemiurus stossichi (Monticelli, 1891) of Luhe (1901) as a possible synonym of H. luehei, Looss (1907, 1908) erected the name H. rugosus for Liihe's material. In agreement with Dawes (1947), Slusarski (1958), Reimer (1970) and others, we can see no reason for retaining H. rugosus as a distinct species. In addition, Slusarski (1958) erected H. raabei as a distinct form which he based on seven specimens from a single salmon in the Baltic Sea. He distinguished it from H. luehei, which he found in the same host and locality, essentially on the basis of a tripartite seminal vesicle (he actually refers to this as a seminal vesicle plus two accessory seminal vesicles) and the presence of narrow, cuticular folds covering the soma and the ecsoma. The latter can easily be dismissed, as these 'folds' are not plications, which never occur on the ecsoma, but small, annular ridges associated with the presence of circular muscle-bands in poorly preserved material. These ridges, which differ markedly from plications (i.e. posteriorly oriented tegumental thickenings), can occur not only in this worm, but also in other species of the genus (Fig. 4E), especially in material which has been slowly fixed in hypo- tonic solutions or frozen prior to fixation: the loss of plications, caused by the expansion of the body, also occurs under these conditions. The apparent presence of a three-lobed seminal vesicle* can possibly also be discounted, as it is clear in some of our whole-mounts that the thin-walled region of the seminal vesicle is often elongate and there are indications that it may possess a medial sphincter. Certainly, sphincters are the usual mechanism for constricting the contents of thin-walled seminal vesicles in other hemiurids. There also appears to be a sphincter present surrounding the region of the distal lobe of the seminal vesicle where it begins to taper towards the pars prostatica (Fig. 7C). Until the presence of a trilocular seminal vesicle as a constant feature is proved beyond doubt, we cannot accept H. raabei as a distinct species. It goes without saying, therefore, that we do not accept Slusarski's subgenus Neohemiurus, which he erected for H. raabei because of the presence of 'cuticular annuli' on the ecsoma. It is worth noting that Rokicki (1973, 1975) claimed to have found two specimens and Gaevskaja (1977) a single specimen of H. raabei in Clupea harengus in the Baltic Sea.
The major taxonomic problem with H. luehei is, however, to prove conclusively that it is distinct from H. appendiculatus. Certainly, one can easily find differences between the two species, such as: (1) H. luehei tends to be much smaller; (2) the plications on the dorsal surface normally extend much further posteriorly in H. luehei; (3) when extruded the ecsoma in H. luehei occupies a smaller proportion of the total body-length, i.e. normally less than one third, as opposed to up to a half; (4) the uterus at the level of the pars prostatica in H. luehei tends to be narrow and relatively straight or sinuous, whereas in H. appendiculatus it is usually swollen with eggs and often loops ventrally to the pars prostatica; (5) the sucker-ratio is slightly smaller in H. luehei; (6) the forebody is slightly shorter in H. luehei; (7) the distance between the seminal vesicle and the ventral sucker is slightly greater in H. luehei in relation to the size of the soma; and (8) there is a host-difference, H. luehei occurring in Clupea harengus, Sprattus sprattus, Sardina
*Despite Slusarski's comments, we still refer to the entire structure as being the seminal vesicle, as this organ is by definition merely a dilation of the vas deferens which acts as a seminal store.
38 D. I. GIBSON & R. A. BRAY
pilchardus and their predators, and H. appendiculatus occurring in Alosa spp. It could be argued that H. appendiculatus is merely an older form of H. luehei, as many of the differences between the two species are consistent with variations and allometry observed in different sizes of specimens in other species of the genus. Similarly, the fact that Alosa spp. tend to live longer than herring, sprats and pilchards may suggest why larger forms occur only in these species, although evidence of the longevity of worms may negate this, and the absence of the larger form in non-clupeid hosts might be because shads do not tend to reach the sea until they are the size of mature sprats, because shads grow to a greater size than the other three clupeids, and because they are not as abundant as the latter. Nevertheless, we have examined very small specimens of//, appendiculatus from Alosa fallax which have features, such as the size of the ecsoma, sucker-ratio and dorsal limit of the plications, which are consistent with those of larger specimens from the same host. Until, therefore, there is experimental evidence to the contrary, we accept H. luehei as a distinct species.
Genus PARAHEMIURUS Vaz & Pereira, 1930
Although Parahemiurus merus (Linton, 1910) is claimed to occur in the south-eastern Baltic Sea (Rokicki, 1973; Gaevskaja, 1977), such records are very questionable. If indeed this species does occur on the eastern side of the Atlantic, its distribution is likely to be restricted to the south of European waters, since most of the records in the literature are from tropical American localities. Fischthal & Thomas (1971, 1972a) have recorded it as occurring off west Africa. Nevertheless, it is worth noting that in the Pacific it is claimed to extend northwards into more temperate waters and has been recorded in the Pacific herring by Arthur & Arai (1980) off British Columbia.
Rokicki (1973) claimed to have found a single specimen of this species in the Baltic herring. He stated that it had an oval seminal vesicle and that the pars prostatica arising from it formed a 'slight expansion' which was 'not like (as) another seminal vesicle'. The presence of an oval rather than a bipartite seminal vesicle is the critical feature distinguishing Parahemiurus from Hemiurus (see Gibson & Bray, 1979). Furthermore, Gaevskaja, who reported (1977) further specimens of this species in Baltic herring, noted (in litt.) that her specimens were similar to Rokicki's in terms of the seminal vesicle and possessed a larger sucker-ratio than that normally found in H. luehei, the usual hemiurid in herring. Nevertheless, she considered that they might be anomalous speci- mens of H. luehei, a suggestion with which we, after examining a specimen which she kindly gave us, strongly concur. A close examination of the latter specimen with DIG microscopy reveals an empty distal lobe of the seminal vesicle and shows that the pars prostatica is replete with spermatozoa.
Subfamily DINURINAE Looss, 1907 Stomachicolinae Yamaguti, 1958.
DIAGNOSTIC FEATURES. Ecsoma well developed; occasionally large. Body-surface plicated or smooth (apparently occasionally striated). Presomatic pit absent. Testes symmetrical to tandem; usually oblique. Seminal vesicle thin- walled; oval to tubular; may be constricted into two to four portions; in forebody, dorsal to ventral sucker or in hindbody. Pars prostatica tubular or vesicu- lar; short or long; may be linked to seminal vesicle by aglandular duct. Sinus-sac present; small or large; usually oval; not enclosing ejaculatory (prostatic) vesicle. Permanent sinus-organ large and muscular, reduced to small papilla or apparently absent. Genital atrium usually well developed; deep or shallow (often depending upon contraction). Ovary usually oval; occasionally reniform or lobed. Terminal portion of uterus may or may not form distinct vesicle just outside sinus-sac. Vitellarium normally seven tubular lobes; three on one side, four on the other. Excretory arms united or not united in forebody. Normally parasitic in stomach of marine teleosts.
Genus DINURUS Looss, 1907
DIAGNOSTIC FEATURES. Body-surface with plications. Seminal vesicle tri-locular (or occasionally quadri-locular); in anterior hindbody or occasionally postero-dorsal to ventral sucker. Pars
HEMIURIDAE 39
prostatica long; may be densely or sparsely invested by gland-cells; linked to seminal vesicle by aglandular duct. Sinus-sac and permanent sinus-organ present; of variable size. Ovary oval. Excretory arms not united in forebody.
TYPE-SPECIES. Dinurus contortus (Rudolphi, 1819) [by original designation].
COMMENT. Although not recorded in our region, it is likely that Dinurus spp., occurring in fishes such as Coryphaena spp. and some of the other warm-water oceanic perciforms, do extend into the southern parts of our study-area. Indeed, Fischthal & Thomas (1972a) claim that D. breviductus Looss, 1907, has been reported in European Atlantic waters.
The relationships of the Atlantic forms of Dinurus were discussed by Gibson (1976). It is also worth noting that this author recorded a species of the related genus Paradinurus Vigueras, 1958, in a gempylid fish off the Canary Isles.
Genus ECTENURUS Looss, 1907
Magnacetabulum Yamaguti, 1934. Parectenurus Manter, 1947.
DIAGNOSTIC FEATURES. Body-surface with plications. Seminal vesicle saccular, tubular or divided into two or three sections; postero-dorsal to ventral sucker or in anterior hindbody. Pars prostatica short (? or missing); connected to seminal vesicle by long, aglandular duct. Sinus-sac and permanent sinus-organ present; small. Ovary oval. Excretory arms not united in forebody.
TYPE-SPECIES. Ectenurus lepidus Looss, 1907 [by original designation].
Ectenurus lepidus Looss, 1907
Ectenurus trachuri Nikolaeva & Kovaleva, 1966, nee (Yamaguti, 1934) Yamaguti, 1970. Ectenurus virgulus Linton of Parukhin et al. (1971) and Nikolaeva (1975).
TYPE-HOST AND LOCALITY. Lichia amia, Adriatic Sea at Trieste, Italy. RECORDS
(i) Material studied
(a) From the NE Atlantic
Trachurus trachurus [?] Kattegat off Frederikshaven, Denmark (Aug., 1976). Collected by M. K0ie. BM(NH) 1983.12.14.1-2.
- [stomach] Bay of Biscay (47°N, 06°W; Mar., 1980). BM(NH) 1983.12.14.3.
(b) From elsewhere
Metacercariae from Sagitta tasmanica [coelom] Off Atlantic coast of NW Africa (Feb., 1975; depth 200 m). Collected by C. Jarling. BM(NH) 1983.10.24.21.
(ii) NE Atlantic records from the literature
Trachurus trachurus [stomach] Aberdeen, Scotland (Sept., 1908). Nicoll (1913: 189). — [stomach] Off W of Scotland (July, 1954). Williams (1960: 708).
- [?] ?NE Atlantic. Gaevskaja & Kovaleva (1980a: 53; 1982: 61).
- [?] North Sea, Bay of Biscay, Straits of Gibraltar. Gaevskaja & Kovaleva (19806: 19).
ASPECTS OF BIOLOGY. Little is known about the biology of this species; but we have identified metacercariae as occurring in a species of Sagitta (see above). This parasite does appear to be most common in the Mediterranean and Black Seas, but occurs in Atlantic waters of western Europe as far north as Scotland and Denmark, although it is not common, thus exhibiting a Lusitanean distribution. It is claimed to occur on the Atlantic coast of Africa as far south as Namibia (see below). In fact its distribution appears to coincide with that of its main host Trachurus trachurus. There have also been a fair number of records in the Mediterranean and Black Sea region from a wide range offish, including Lichia amia, Trachynotus ovatus, Atherina hepsetus, A. boyeri, Cepolamacrophthalma, Pomatomussaltator, Lophius piscatorius , L. budegassa, Spicara maena, S. smarts, Scomber japonicus, Trachipterus trachypterus , Caranx rhonchus, Scyris alexandrina and Selar djeddaba. Ectenurus spp. are generally considered to be parasites of
40 D. I. GIBSON & R. A. BRAY
carangids. In the above list Trachurus, Lichia, Trachynotus, Caranx, Scyris and Selar are carangids, but Cepola, Pomatomus and Spicara are all related members of the Percoidei. Some hosts, e.g. Lophius spp., are presumably accidental, the worms having been taken in with their prey.
PREVIOUS DESCRIPTIONS. Looss (1908: 124; brief, but well illustrated); Vlasenko (1931: 118); Janiszewska (1953: 31; a few measurements only); Mazza (1963: 447; brief); Nikolaeva (1963: 410; brief, no figure; 1966: 53; some measurements only); Nikolaeva & Kovaleva (1966: 67; as E. trachuri).
DESCRIPTION. (Fig. 8). This description is based upon two flattened and one unflattened whole- mounts from fishes and two metacercariae from chaetognaths. As no sections were seen our interpretation is based upon these worms with occasional reference to the figures of Looss (1908). The measurements are given in Table 5.
The body-surface of these cylindrical to fusiform worms is almost entirely covered by shallow, transverse plications. They are absent from the ecsoma, but reach back laterally on the soma to a distance about half-way between the ovary and the posterior extremity of the soma. Ventrally they extend almost to the posterior limit and dorsally they reach to about the level of the ovary. These levels would be expected to vary with the state of contraction of the worm. In the forebody of flattened specimens the plications may not be visible, apart from the regions dorsally and later- ally to the oral sucker. The ventral sucker is also surrounded by plications. In the metacercariae the plications are more easily seen and tend to extend further posteriorly. In all our specimens the ecsoma is everted, except in the case of the metacercariae where it is withdrawn and not fully formed. The oral sucker is small, with the result that the forebody is conical. It is ventrally sub- terminal and surmounted by an indistinct pre-oral lobe. In material fixed in formalin and other cold fixatives (with the exception of GAA and Borland's fluid) the anterior part of the body is usually curved ventrally, thus bringing the two suckers into close proximity and emphasizing the two muscular thickenings which occur dorso-laterally to the oral sucker (see Fig. 8B and the figures of Looss, 1908). In extended specimens without the ventral flexion of the body, these thickenings, which do appear to be a feature of the worm, can only be seen as oval patches of muscle just beneath the dorso-lateral surface of the body. Any protrusions caused by these muscular thickenings are probably transitory. There is a distinct pattern of papillae surrounding the aperture of the oral sucker visible in our unflattened specimens (Fig. 8E). The ventral sucker is very large and is normally within the anterior third of the body. The sucker-ratio is usually in the region of 1 : 2-5-3-5. As it is 1 : 2-5 in our smallest specimen, allometry may be involved.
There is no prepharynx. The muscular pharynx leads into a short, saccular oesophagus which appears to pass postero-laterally and join a commissure linking the two 'Driisenmagen'. The caeca then pass posteriorly in the dorso-lateral fields and end blindly deep within the ecsoma when the latter is everted.
The excretory pore opens terminally on the ecsoma. According to our material, the first part of the stem of the Y-shaped excretory vesicle within the ecsoma (Fig. 8A) may be saccular with a 'papillate' lining, and the remainder of the stem appears to be tubular. According to Looss (1908) the stem divides at the level of the posterior margin of the ventral sucker, and the two arms end blindly lateral to the oral sucker. Although we have no sectioned material, our whole-mounts also indicate that the arms end blindly.
Two oval testes occur obliquely in the ventral field a short distance posterior to the ventral sucker. (Our unflattened whole-mount (Fig. 8D) is abnormal in that the anterior testis is very small and contains no stainable material.) The vasa eflferentia cannot be seen in our specimens, but presumably they unite as they join the tripartite seminal vesicle, which occurs between the testes and the ventral sucker. The proximal and largest part of the seminal vesicle is globular to oval. It is separated by a constriction from the slightly smaller middle section, which is similarly shaped. The third part is tear-shaped and tapers distally to form a simple duct. The constriction between the middle and third parts is not always distinct. The aglandular duct is an unmodified region of the ejaculatory duct (often referred to as an aglandular region of the pars prostatica). It
HEMIURIDAE
41
Fig. 8 Ectenurus lepidus ex Trachurus trachurus. (A) Flattened worm from Denmark; (B) Anterior extremity (curved ventrally) showing muscular pads; (C) Male terminal genitalia of flattened worm; (D) Small specimen from Bay of Biscay; (E) Anterior region of small specimen. Scale bars: A 500 /mi; C 100 /mi; D 200 //m; E 100//m.
42 D. I. GIBSON & R. A. BRAY
Table 5 Measurements of Ectenurus lepidus
|
Authority |
Looss (1908) |
Nikolaeva (1963) |
Mazza (1963) |
Present material |
|
Host |
Lichia amia |
Trachurus |
Trachurus |
Trachurus |
|
mediterraneus |
trachurus |
trachurus |
||
|
Locality |
Trieste, Italy |
Mediterranean |
French |
Kattegat |
|
Mediterranean |
||||
|
Length (mm) |
up to 2-0 |
1-68-2-28 |
1-72 |
2-2-2-7 |
|
Breadth (mm) |
0-25-0-3 |
0-31-0-34 |
0-41 |
0-5-0-6* |
|
Ecsoma (mm) |
- |
- |
- |
0-45-0-5 |
|
Forebody (mm) |
- |
- |
- |
0-3-0-4 |
|
Oral sucker (mm) |
0-08-0-1 2 diam. |
0-7-0-1 Ix |
0-09 x 0-07 |
0-12x0-11-0-13 |
|
0-08-0-11 |
||||
|
Ventral sucker |
0-2-0-3 diam. |
0-1 7-0-22 x |
0-29 diam. |
0-35-0-36 diam. |
|
(mm) |
0-2-0-32 |
|||
|
Sucker-ratio |
>1:2 |
(1 : 3-4) |
- |
1 : 2-7-3-2 |
|
Testes (mm) |
- |
0-07-0- 13 x |
0-14x0-15 |
0-1 7-0-23 x |
|
0-08-0-31 |
0-2-0-25 |
|||
|
Ovary (mm) |
- |
0-12-0- 13 x |
0-1x0-14 |
0-1 3-0-2 x |
|
0-13-0-16 |
0-21-0-26 |
|||
|
Eggs (/mi) |
20x10 |
16-25x10-12 |
18-22x11-13 |
16-19x7-10 |
|
(usually 17-18x |
||||
|
8-9) |
Measurements in parentheses are calculated from figure. *Flattened specimens.
is long and leads into the forebody dorsally to the ventral sucker. Inside the forebody the distal extremity of the duct forms a typical pars prostatica, i.e. it is surrounded by gland-cells and lined by anuclear blebs (Fig. 8C). The length of the pars prostatica in relation to the total length of the duct is difficult to judge in these specimens, but it must be in the range of 15-20 %. Although perhaps marginally wider than the remainder of the duct, the pars prostatica in our material is tubular and not vesicular, as figured by Looss (1908). Distally the pars prostatica opens into the base of a stout, oval to elongate oval sinus-sac, within which it immediately unites with the metraterm to form the hermaphroditic duct. The proximal region of this duct within the sinus-sac appears to have a thick, rugate or villous lining; but distally, where it passes through a stout, conical, permanent sinus-organ, it is a narrower, simple tube (this is more obvious in Looss' (1908) figures). The sinus-organ occurs within a deep genital atrium, which appears to open to the exterior mid-ventrally close to the ventral margin of the oral sucker. In the flattened specimens the sinus-sac, together with the sinus-organ, appears on superficial examination to form an oval structure ventrally in the forebody, which has a length similar to that of the oral sucker. In our unflattened specimen the sinus-sac is more elongate (Fig. 8D); but the sinus-organ is small. This difference may possibly be due to the relaxation of the muscles of the sinus-sac brought about by GAA fixation, as opposed to the contraction caused by formalin: hence the difference in size of the sinus-organ. It is important to remember that in worms like this, where the sinus-organ and sinus-sac are similar in size, the size of one must to some extent be a function of the size of the other. The position of the sinus-complex varies with the degree of contraction of the forebody and the genital atrium; but it normally occurs between the level of the anterior margin of the pharynx and the anterior margin of the ventral sucker.
The transversely oval ovary occurs ventro-laterally on either side of the body just anterior to the middle of the hindbody, although its position presumably depends upon the degree of con- traction and the amount of evertion of the ecsoma. It may be slightly larger or slightly smaller than the testes, from which it is usually separated by loops of the uterus and/or lobes of the
HEMIURIDAE 43
vitellarium. The oviduct appears to leave the ovary postero-dorsally to join the Mehlis' gland - Juel's organ complex, which, although not clearly visible in our whole-mounts, appears to be similar to that of other hemiurids. The first coils of the uterus, immediately posterior to the latter complex, form a uterine seminal receptacle. The uterus then appears to loop back usually into the proximal region of the ecsoma, although not to the same extent as the caeca. It then loops for- ward on the side of the body opposite to the ovary past the ovarian complex, where it fills much of the available space in the remainder of the hindbody, often looping between the ovary and the hind-testis and passing dorsally to the testes. Dorsal to the ventral sucker it passes forward more directly, gradually narrowing, until it forms a narrow, tubular metraterm, which is of similar length to the pars prostatica, prior to entering the base of the sinus-sac where it unites with the male duct. The uterus is filled with numerous small, operculate eggs. The vitellarium is composed of seven digitiform lobes, which are arranged such that three lobes arise from one lateral collect- ing duct and four from the other. These short collecting ducts unite ventrally immediately posterior to the level of the ovary. The ducts are in fact so short that the seven lobes may appear superficially to have a rosette-like arrangement. The lobes are at least six times as long as they are wide, and occur in the ventral and lateral fields in the ovarian region, often crossing the ovary ventrally and lying between the ovary and the posterior testis (Fig. 8A, D). Presumably, a short common duct connects the transverse collecting ducts with the oviduct.
DISCUSSION. Ectenurus lepidus is a parasite primarily of carangids, but it has been recorded from other groups of fishes, although mainly from members of the suborder Percoidei. Despite the fact that Lichia amia is the type-host, the majority of records have been from Trachurus spp. The only piscine host in the NE Atlantic, Trachurus trachurus, is unusual, when compared with the majority of teleosts in the region, in that it appears to have its own peculiar helminth-fauna.
According to the literature, E. lepidus has a widespread distribution outside European waters. In our opinion, however, this requires confirmation. Manter (1954), although noting that his specimens had a longer sinus-sac than that described by Looss (1908), claimed to have found it in Helicolenus papillosus (=percoides) and Trachurus novaezelandiae (possibly a synonym of T. dedivis) in New Zealand waters. Manter believed that the 'short and thick' sinus-sac figured by Looss was 'in a contracted state'. The shape of the sinus-sac in our flattened, formalin-fixed material appears to be identical to that described by Looss. Until we obtained a small, unflattened specimen fixed in GAA, we believed that the short, broad sinus-sac was a distinctive feature of E. lepidus. We are now tending to believe that Manter's observation was correct, for, although this small specimen possesses a much more elongate sinus-sac, marginally larger eggs and a smaller sucker-ratio than our two flattened specimens, it appears to be within the limits of the species as described in the literature and possesses 'muscular thickenings' dorso-lateral to the oral sucker. We are, therefore, treating all of our specimens as being conspecific. In relation to Manter's New Zealand record, it is worth noting that Korotaeva (1975) did not find E. lepidus in Trachurus dedivis in the Great Australian Bight, but claimed to have found E. virgula Linton, 1910, a species with a long sinus-sac. It is also worth mentioning that E. antipodus (Lebedev, 1968) has been recorded from a carangid, as has E. helicoleni (Lebedev, 1968) from Helicolenus papillosus in the Tasman Sea (the latter species is also claimed to occur in Brama brama off Mauritania - see Szuks, 1981).
Travassos et al. (1967) claimed to have found E. lepidus in Oligoplites saurus off the Atlantic coast of Brazil at Santa Cruz; but, according to their description, it has a long 'cirrus-sac' reach- ing to the posterior margin of the ventral sucker. In our opinion it more closely resembles E. virgula. A neighbouring species, E. rodriguesi, described by Cristofaro & Guimaraes (1974) from Gymnothorax vicinus appears to be a synonym of Lecithodadium havanensis (Vigueras, 1958). In our opinion, therefore, it seems unlikely that E. lepidus occurs on the western side of the North Atlantic. The common forms in the Gulf of Mexico are E. virgula, characterized by a very long, narrow sinus-sac, and E. americanus (Manter, 1947), a form similar to E. lepidus, but with a much smaller sucker-ratio. We have examined the specimens from Caranx ruber off Bermuda, which were designated E. virgula by Rees (1970), and consider them to be E. americanus. E. chloroscombri (Siddiqi & Cable, 1960) is very similar to, and probably synonymous with, E. virgula.
44 D. I. GIBSON & R. A. BRAY
Both Manter & Pritchard (19606) and Yamaguti (1970) claim that E. lepidus occurs in carangids off Hawaii. Manter & Pritchard noted that the sinus-sac is elongate and Yamaguti's figure clearly shows it to be quite a different shape to that of European specimens of E. lepidus. The Hawaiian form is similar to E. selari (Parukhin, 1966) from a carangid in the Gulf of Tonkin, which in turn is similar to E. trachuri (Yamaguti, 1934) nee Nikolaeva & Kovaleva, 1966, from a carangid off Japan. It is worth noting that E. selari and E. trachuri are very similar in morphology and occur in similar hosts to E. virgula, and that all three of these species are claimed to have been found off the Cape Verde Islands by Szuks (1981).
E. lepidus is also claimed to occur in carangids off the west coast of Africa by Kovaleva (19686) [Namibia], Fischthal & Thomas (1971) [Ghana], Siddiqi & Hafeezullah (1975) [Nigeria] and Szuks (1981) [Cape Verde Islands and Mauritania]. Kovaleva recorded it from Trachurus trachurus capensis, but did not describe it. Fischthal & Thomas recorded it from Chloroscombrus chrysurus, Decapterus rhonchus and Galeoides decadactylus, and, although they gave no description, they compared it with specimens of 'E. lepidus' from Hawaii, the material of Manter & Pritchard (19606), and with the type-specimen of E. chloroscombri, which they consider synonymous with E. lepidus (but see above). They found all of this material to be 'basically alike'. Siddiqi & Hafeezullah (1975) provided a very brief description and a very small figure of one specimen from Chloroscombrus chrysurus. Although their specimen resembles E. lepidus, its description is not detailed enough for us to be certain of its identity; but the sinus-sac appears to be quite a different shape to that described for E. chloroscombri on the other side of the Atlantic. Szuks (1981) recorded E. lepidus from Euthynnus alleteratus, Trachurus trecae, T. trachurus and Lutjanus agennes, but did not describe or discuss the worms. He also quoted unpublished records from Scomber japonicus ( = colias) and Decapterus rhonchus from off NW Africa.
In addition to the above records, Parukhin & Solonchenko (1967) briefly described, but did not figure, E. lepidus from Selar crumenophthalmus in the Gulf of Aden. Parukhin (19766; 1978) also claimed to have found this species and E. virgula in the Gulf of Aden and E. virgula (spelled vulgaris in error in 1978) and E. americanus in other parts of the Indian Ocean. Parukhin & Solonchenko's description omits mention of the shape of the sinus-sac, so the worms' identity requires confirmation; but we have been able to confirm the presence of E. virgula in Selar crumenophthalmus in the Indian Ocean region from specimens from Pinang, Malaysia, housed in the collection of the BM(NH).
In 1931 Vlasenko described material from Trachurus trachurus (the fish may well have been T. mediterraneus, as only in recent years has this been recognized as a distinct species) in the Black Sea, which he thought were questionable specimens of E. lepidus. Vlasenko considered that they differed from E. lepidus of Looss (1908) in: (1) the shape of the vitellarium; (2) the length of the caeca; (3) the form and size of the ovary; (4) the absence of 'thickenings' lateral to the oral sucker; and (5) the ventral sucker being three times larger than the oral sucker. Although several workers, such as Osmanov (1940), Butskaja (1952), Pogorel'tseva (1952), Chernyshenko (1955) and even Kovaleva (1968 a,b), have continued to refer to specimens from the Black Sea as E. lepidus, Nikolaeva & Kovaleva (1966), Kovaleva (1969, 1970a,6) and Nikolaeva & Parukhin (1969) have considered that Vlasenko's material and their own specimens from T. mediterraneus were a distinct species, E. trachuri Nikolaeva & Kovaleva, 1966, nee E. trachuri (Yamaguti, 1934). They distinguished it from E. lepidus on: (1) the large size of the ventral sucker (ratio 1 : 3-4); (2) the ovary is larger than the testes rather than smaller; (3) the 'thickenings' lateral to the oral sucker are absent; and (4) the caeca extend well into the ecsoma. Later, Parukhin et al. (1971) and Nikolaeva (1975) considered this species to be a synonym of E. virgula. Nikolaeva distinguished it from E. lepidus by: (1) the small size of the pre-oral lobe; (2) the absence of 'thickenings' lateral to the oral sucker; (3) the large size of the ventral sucker; and (4) the large size of the ovary. In fact, the size and shape of the sinus-sac preclude any consideration of E. trachuri of Nikolaeva & Kovaleva (1966) as a synonym of E. virgula. In agreement with Fischthal & Thomas (1971), we consider it to be a synonym of E. lepidus, because many of the differences listed above can be considered within the range of intra-specific variation. The confusion results from the fact that Looss' description has been the only available detailed picture of E. lepidus (sensu stricto). Considering each of Nikolaeva's points in turn: (1) although their material does
HEMIURIDAE 45
appear to have a greater sucker-ratio than our material and that of Looss (1908), that of Mazza (1963) extends well into their range: in addition, one of our specimens has a ratio almost identical to that reported by Vlasenko (1931) and another is greater than 1 : 3; (2) the ovary in one of our two flattened specimens is larger than the testes; (3) the 'thickenings' lateral to the oral sucker would appear to be transitory or often inconspicuous; and (4) the caeca in our specimens extend well into the ecsoma.
Subfamily ELYTROPHALLINAE Skrjabin & Guschanskaja, 1954 Musculovesiculinae Skrjabin & Guschanskaja, 1954.
DIAGNOSTIC FEATURES. Ecsoma well developed. Body-surface smooth or plicated. Presomatic pit absent, but ventro-cervical groove often present. Testes tandem to symmetrical, usually oblique. Seminal vesicle with exceptionally thick, muscular wall; oval, not constricted into portions; in forebody, dorsal to ventral sucker or in hindbody. Pars prostatica tubular; long or short; usually linked to seminal vesicle by short, aglandular duct. Sinus-sac commonly tubular, long, not enclosing ejaculatory (prostatic) vesicle. Sinus-organ usually well developed, but delicate and amuscular. Genital atrium usually deep (depending upon contraction). Ovary oval. Eggs rarely filamented. Vitellarium seven tubular to tear-shaped lobes, three on one side, four on the other, which may form rosette. Excretory arms united in forebody. Parasitic mainly in stomach of marine teleosts.
Genus LECITHOCLADIUM Liihe, 1901
Magnapharyngium Bilqees, 1971. Colletostomum Sahai & Srivastava, 1978. Clefticolletta Sahai & Srivastava, 1978.
DIAGNOSTIC FEATURES. Body-surface with plications. Oral sucker often funnel-shaped. Pharynx elongate. Seminal vesicle large; in hindbody. Pars prostatica long and sinuous; mainly or entirely in hindbody. Sinus-sac tubular; narrow; not reaching level of seminal vesicle and usually entirely or mainly in forebody. Vitelline lobes long and tubular. Parasitic in stomach of marine teleosts.
TYPE-SPECIES. Lecithocladium excisum (Rudolphi, 1819) [by original designation].
Ledthocladium excisum (Rudolphi, 1819) Lime, 1901
Distoma excisum Rudolphi, 1819.
Fasciola excisum (Rudolphi) de Blainville, 1828.
Distoma (Crossodera) excisum (Rudolphi) Dujardin, 1845.
Distoma (Apoblema) excisum (Rudolphi) Stossich, 1886.
Apoblema excisum (Rudolphi) Juel, 1889.
Hemiurus excisus (Rudolphi) Looss, 1899.
Distoma (Lecithocladium) excisum (Rudolphi) Cohn, 1902.
Crossodera excisum (Rudolphi) Seurat, 1909.
IDistomum crenatum Molin, 1859.
? 'Apoblema crenata (Molin) Juel, 1889.
1 Lecithocladium crenatum (Molin) Looss, 1907.
Lecithocladium excisiforme Cohn, 1903.
Distomum gulosum Linton of Johnstone (1906).
1 Lecithocladium 'exiguus' of Radulescu (1969) [nom. nud. or error pro 'excisum'].
TYPE-HOST AND LOCALITY. Scomber scombrus, Rimini, Italy. RECORDS
(i) Material studied (a) From the NE Atlantic
Scomber scombrus [stomach] Plymouth, Devon, England. Material of Baylis & Jones (1933: 631). BM(NH) 1932.12.6.10. Material collected by P. G. Corbin. BM(NH) 1937. 6.8.142-150.
46 D. I. GIBSON & R. A. BRAY
[stomach] Off W of Scotland (56°N, 08°W; depth 120m; July, 1954). BM(NH) 1959.10.14.26.
(Material of Williams, 1960: 708).
- [stomach] Off coast of Portugal (40°N, 10°W; depth 256-290 m; Jan., 1971). BM(NH) 1973.5.17.63-65. (Material of Bray, 1973: 178). - [stomach] Off Faeroe Isles (62°N, 08°W; July, 1976). BM(NH) 1983.12.14.4.
[stomach] Off St. Andrews, Scotland (July, 1949). Collected by D. D. R. Burt. BM(NH)
1983.12.14.5-8.
[stomach] Bay of Biscay (45°N, 02°W; depth 76-80 m; March, 1980). BM(NH) 1983.12.14.9.
Trachurus trachurus [?] Kattegat off Frederickshaven, Denmark. Collected by M. K0ie. BM(NH) 1983.12.14.1-2.
(b) From elsewhere
(?) Centrolophus niger [stomach] Bordighera, Italy (removed from fish in BM(NH)). BM(NH) 1984.7.27.96
( = ? L. crenatum (Molin)). Scomber japonicus [stomach] Atlantic coast of Morocco (34°N, 09°W; depth 222-236 m; Jan., 1971).
BM(NH)1983.12.14.10.
(ii) NE Atlantic records from the literature
? Scomber japonicus [?] North or South Atlantic. Radulescu (1969: 80; as 'L. exiguus').
Scomber scombrus [stomach] Off Ireland. Bellingham (1844: 425; as Distoma excision).
— [intestine] (Rennes), Brittany, France. Dujardin (1845: 436; as Distoma (Crossoderd) excisum).
— [stomach] Varberg, Sweden (June, Aug., Sept.) Olsson (1868: 51; as Distoma excisum).
— [stomach] Aalesund, Sweden. Olsson (1868: 51; as D. excisum).
— [stomach] Bergen, Norway (Jul., Aug.). Olsson (1868: 51; as D. excisum).
— [stomach] Bohuslan, Sweden (July). Olsson (1876: 21; as D. excisum).
— [stomach & intestine] Belgian coast, van Beneden (1871: 37; as D. excisum).
- [stomach & intestine] Kristineberg, Sweden. Juel (1889: 5; as Apoblema excisum); (July) Lonnberg (1889: 56; as D. excisum).
- [?] Off Walney Island, Irish Sea (July, 1905). Johnstone (1906: 319; as Distoma gulosum).
- [stomach] Millport, Firth of Clyde, Scotland. Nicoll (1910: 349).
- [stomach] Aberdeen, Scotland. Nicoll (1913: 189).
[stomach] Plymouth, Devon, England. Nicoll (1914: 485); Baylis & Jones (1933: 631); Baylis (1939:
478).
- [stomach] W of Scotland (June, 1954). Williams (1960: 708).
- [stomach] Portugese coast (40°N, 10°W; depth 256-290 m; Jan., 1971). Bray (1973: 178). [stomach] St Andrews, Scotland. Gordon, in Laverack & Blackler (1974: 35).
This species was also recorded probably just to the south of our region (the actual locality was not given) in Scomber japonicus, S. scombrus, Trachurus trachurus and Caranx rhonchus by Jessen (1975: 179).
ASPECTS OF BIOLOGY. Little is known about the biology of this species. The metacercariae probably occur in ctenophores and possibly other planktonic animals, as Boyle (1966) recorded five specimens of a species of Lecithocladium (he called it L. excisum: see below) from the ctenophore Pleurobrachia pileus in New Zealand waters and Reimer (1976) reported six records of a worm which he considered to be a species of Lecithocladium from Pleurobrachia globosa off Madras, India. Reimer (1976) also reported two other records in the same locality from Janthina globosa, a gastropod mollusc which lives on ctenophores and coelenterates.
The main host for the adult in our region is Scomber scombrus; but it also occurs in S. japonicus. There are also records in the literature from a wide range of other fishes outside our region; but, as discussed below, many of these records require confirmation. We have specimens from the carangid Trachurus trachurus, but they are immature. Looss (1908) also recorded immature forms from this host in the Mediterranean Sea, and a very low prevalence was reported by Parukhin et al. (1971) also from the Mediterranean. It is also said to occur in Trachurus mediterraneus from the Mediterranean and Black Seas (Nikolaeva, 1963; Nikolaeva & Kovaleva, 1966; Kovaleva, 19706; Parukhin, 1976). It would appear, therefore, that while Scomber spp. are the main hosts, it may occasionally occur, often as an immature form, in other fishes, such as carangids, which occupy a similar ecological niche and which may feed on ctenophores. The distribution of L. excisum is dealt with in the 'Discussion'.
HEMIURIDAE 47
PREVIOUS DESCRIPTIONS. Dujardin (1845: 436; as Distoma (Crossodera) excisum; brief); Juel (1889: 8; as Apoblema excisum; parts of body only); Johnstone (1906: 319; as Distoma gulosum); Cohn (1903: 54; as L. excisiforme; brief); Looss (1908: 125; detailed figures); Markowski (1933: 18); Timon-David (1937: 16); Janiszewska (1953: 31; measurements only); Mazza (1963: 447; measurements and figures); Koval & Otsupok (1964: 50; measurements only); and Hadzhiiski (1980: 150; figure and a few measurements). It has also been described in the region of Japan by Yamaguti (1934: 479; measurements only); Zhukov (1960: 39; figure and a few measurements); and Ichihara et al. (1968: 49).
DESCRIPTION. (Figs 9 & 10). This description is based upon 21 whole-mounts and one obliquely sectioned specimen. The body is tubular, with a truncate anterior end and, usually, a conical posterior end, the latter being caused by the ecsoma which is usually protruded. The protruded ecsoma may comprise up to slightly more than half of the total length of the worm. In some speci- mens a double invagination of this organ may occur. Much of the somatic surface is covered with distinct annular plications; but these are absent on the ecsoma, ventrally between the suckers and surrounding the caudal extremity of the soma: they may extend slightly further posteriorly and be slightly more distinct on the ventral surface than on the dorsal. The plications are often quite widely spaced, especially on the dorsal surface, and they may be slightly crenulate. Dorsal to the pharynx is a distinct region where the plications are accentuated and much more deeply crenulate (Fig. 10A): this region is referred to by Looss (1908) as the 'Krauselung' and is a very distinctive feature of this species, although it is not always visible in poorly fixed, frozen or flattened material. There is no sign of the muscular protrusion ('Nacken-buckel') dorsal to the oral sucker which is a distinctive feature of the related species L. cristatum (Rud., 1819) in unflattened material. There is no presomatic pit. Measurements of this species are given in Table 6.
The oral sucker is terminal, there being no pre-oral lobe; but the aperture may be oriented ventrally associated with a ventral flexion of the forebody. It is a large, muscular and infundibuli- form organ, which is distinctly cleft on each ventro-lateral margin (Fig. 9A,B). The globular ventral sucker is smaller than the oral sucker: the ratio (width) is usually in the region of 1 : 0-8-0-9. In fully-developed worms it occurs within the first quarter of the soma, but in immature worms the forebody occupies a larger proportion of the body. The aperture of the ventral sucker tends to be oriented slightly antero-ventrally.
There is no prepharynx. the muscular pharynx is very large and elongate, often extending past the anterior margin of the ventral sucker. Posteriorly it gives rise to a short, oval and muscular oesophagus from which two relatively narrow, muscular arms arise dorso-laterally. These short ducts, which are lined with claviform, villous projections, pass antero-laterally to unite with the caeca. The latter gradually widen and almost immediately reflex and pass posteriorly, thus form- ing distinct 'shoulders'. There are no 'Driisenmagen' visible in our material, although we have observed indistinct organs in the related L. cristatum. The relatively broad caeca pass back in the dorso-lateral fields and terminate blindly close to the distal extremity of the ecsoma.
The excretory pore is situated ventro-terminally on the ecsoma. The tubular, Y-shaped excretory vesicle has a smooth, vesicular lining and a muscular wall in the posterior region; but, in our sectioned specimen, at about one- third of the way along the ecsoma, the wall becomes very fluted, and about half-way along the ecsoma there is a distinct muscular sphincter, after which the vesicle has a more typical appearance. It continues forward medially into the soma between the coils of the uterus, running dorsally to the gonads, and bifurcates at about the level of the anterior margin of the anterior testis. The two arms continue forward in the dorso-lateral fields into the forebody, where they taper at about the level of the anterior half of the pharynx to become narrow ducts. In our sections these appear to gradually fade away; but Yamaguti (1934) claimed that in his live material and whole-mounts the arms were united dorsally to the oral sucker. Looss (1908) also found no connection between the ducts. Such a connection does normally occur in elytrophallines; but it is possible that in this instance the connecting duct, if present, is extremely fine.
The two oval testes occur almost symmetrically to tandem in about the middle of the soma, but their exact position varies considerably with the state of contraction or eversion of the ecsoma.
48
D. I. GIBSON & R. A. BRAY
Fig. 9 Lecithocladium exciswn ex Scomber scombrus. (A) Flattened worm; (B) Unflattened worm; (C) Section of Mehlis' gland- .Fuel's organ complex. Scale bars: A,B 1 mm; C 100 //m.
HEMIURIDAE
49
Fig. 10 Lecithocladium excisum ex Scomber scombrus. (A) Anterior region of laterally mounted, flat- tened worm; (B) Distal part of terminal genitalia; (C) Plications across surface dorsal to pharynx ('Krauselung'). Scale bars: A 500 ^m; B 100//m; C 200 /mi.
50 D. I. GIBSON & R. A. BRAY
Table 6 Measurements of Lecithocladium excisum from Scomber scombrus
|
Authority Locality |
Looss(1908) HYieste, Italy |
Mazza (1963) French Mediterranean |
Koval & Otsupok (1964) Black Sea |
Present material NE Atlantic |
|
Length (mm) |
3-8 |
2-92^-85 |
5-8 |
3-5-7-2 |
|
Breadth (mm) |
0-5-1 |
0-52-0-81 |
- |
0-6-1-2 |
|
Ecsoma (mm) |
- |
0-64-1-03 |
- |
0-15^-0 |
|
Forebody (mm) |
- |
- |
- |
0-6-0-11 |
|
Oral sucker (mm) |
0-65x0-5 |
0-1-0-14 x |
0-33-0-63 x |
0-35-0-65 x |
|
0-31-0-48 |
0-37-0-67 |
0-38-0-6 |
||
|
Ventral sucker |
0-35-0-45 |
0-23-0-34 x |
0-33-0-49 x |
0-3-0-47 x |
|
(mm) |
diam. |
0-26-0-35 |
0-35-0-56 |
0-35-0-5 |
|
Sucker-ratio |
- |
- |
- |
1 : 0-72-0-95 |
|
Testes (mm) |
- |
0-26-0-27 x |
0-1 5-0-29 x |
0-23-0-42 x |
|
0-34-0-4 |
0-13-0-37 |
0-23-0-43 |
||
|
Ovary (mm) |
- |
0-24-0-33 x |
0-1 3-0-27 x |
0-15-0-3 x |
|
0-17-0-26 |
0-33-0-35 |
0-28-0-39 |
||
|
Eggs (//m) |
20-22 x 10-12 |
20-22x10-12 |
19-20x10-13 |
21-24x11-14 |
|
(usually 22-23 x |
||||
|
12-13) |
When oblique, either the left or the right testis may be the more anterior, and the anterior testis is usually slightly more ventrally situated than the other. In our sectioned specimen the vasa efferentia are very short (c. 100 um); but, judging by the variable position of the testes, they must be very contractile. They leave the testes anteriorly and unite almost immediately to form the seminal vesicle. This is a very large, fusiform structure with an extremely thick, muscular wall. It normally extends anteriorly from the testes obliquely to a level about half-way between the testes and the ventral sucker. The posterior extremity is usually more sinistrally and ventrally situated than the anterior extremity. Distally the seminal vesicle gives rise, via a short, aglandular duct, to the pars prostatica, which is very long. The proximal three-quarters of the pars prostatica in our material are broad, muscular, convoluted, surrounded by a dense, broad band of large gland- cells, and appear to possess a smooth lining and a lumen filled with spermatozoa. ( It is worth noting that in L. cristatum the lining is more typical in that it bears the usual 'transitory' blebs which are assumed to arise from the outer gland-cells.) Most of this region of the pars prostatica occurs ventrally between the seminal vesicle and the ventral sucker. At about the level of the middle of the ventral sucker the pars prostatica straightens, narrows slightly, becomes relatively thin-walled, loses its broad band of external gland-cells and acquires a narrow, diffuse, external band of globular, non-staining cells (Fig. 10A). At this point a more typical lining develops, i.e. globular, non-staining blebs, which are often apparently ruptured. In this instance the typical external cells appear, therefore, to be physically separated from the internal blebs. This is difficult to explain, but it is possible that there are two kinds of cells in the pars prostatica of all hemiurids and that it is the small, non-staining cells that form the internal blebs. As there is no evidence of the blebs in the proximal part of the pars prostatica, it is unlikely that they have migrated down the duct. In the posterior forebody or often antero-dorsally to the ventral sucker in smaller worms, the pars prostatica unites with the metraterm as they enter the base of the sinus-sac. The length of the narrow, cylindrical sinus-sac varies, usually being longer than the pharynx in small worms and slightly shorter in large worms. Its position is also variable due to the fact that the wall of the genital atrium is very contractile, so the position of its posterior extremity varies between a level antero-dorsal to the ventral sucker and just anterior to the middle of the pharynx. The anterior extremity of the sinus-sac is often very difficult to elucidate, as in many whole-
HEMIURIDAE 51
mounts it appears to grade into the wall of the genital atrium. One feature which indicates the whereabouts of the junction between the wall of the sinus-sac and that of the genital atrium is a bunch of small gland-cells which surround it (Fig. 10B): this feature was also noted by Gibson (1976) in the related L. cristatum and Elytrophalloides oatesi (Leiper & Atkinson, 1914). Within the sinus-sac the hermaphroditic duct is initially straight or sinuous, but the distal third of its length may be much more sinuous or slightly convoluted. Within the genital atrium the hermaphroditic duct is everted to form a small, amuscular sinus-organ (Fig. 10B); but this is very difficult to see in many specimens. It is possible that it is a temporary feature in this species, but it is likely, as in other members of the subfamily, that it is very variable in size. The genital atrium is very variable in length, but its junction with the sinus-sac is usually ventral to the oral sucker. The genital pore occurs mid-ventrally immediately posterior to the ventral margin of the oral sucker.
The oval ovary occurs mid-ventrally in the posterior half of the somatic hindbody, usually being separated from the testes by loops of the uterus. Even in our most extended specimens the ovary does not penetrate the ecsoma. Immediately posterior to the ovary, Juel's organ and Mehlis' gland form a large, oval complex which is distinctly delimited from the surrounding parenchyma by a layer of connective tissue (Fig. 9C). Juel's organ includes a large 'inner vesicle' containing many spermatozoa, which has caused several authors to consider it to be a seminal receptacle. The short oviduct leaves the ovary postero-medially, enters the proximal female com- plex and almost immediately receives the duct from Juel's organ and the common vitelline duct. The ootype is tubular and winds through the mass of gland-cells which form Mehlis' gland. On leaving the complex the first coils of the uterus are filled with spermatozoa and thus form a uterine seminal receptacle. The initial coils loop posteriorly, extending deep into the ecsoma, although not nearly as far as the caeca. In specimens with a withdrawn ecsoma the uterine coils may be retained in the soma (Fig. 9B). The coils then reflex and return anteriorly mainly on the opposite side of the body to that in which they have descended, passing laterally to the ovary, but extending across the body between the ovary and the testes. The coils then tend to run dorso- laterally to the testes on the opposite side of the body to that on which they passed the ovary and then fill much of the region dorsal to the seminal vesicle and pars prostatica. Dorsally or postero- dorsally to the ventral sucker the uterus tapers to form a narrow, muscular metraterm, which continues forwards directly to unite with the male duct as they pass through the base of the sinus-sac. The uterus is filled with numerous small, operculate eggs. Occasionally spermatozoa may be seen filling portions of the distal uterus.
The vitellarium is composed of seven long, tubular lobes which unite postero-ventrally to the ovary and ventrally to the Mehlis' gland - Juel's organ complex. The lobes, which are arranged with three on one side of the body and four on the other, extend around the worm in the dorso- lateral fields, reaching between the levels of the posterior margin of the testes and the middle of the ecsoma.
DISCUSSION. Lecithocladium excisum was first recorded by Rudolphi (1819) from Scomber scombrus at Rimini on the Adriatic coast of Italy and from S.japonicus at Naples. Subsequently, it has been recorded frequently from these fishes, in particular S. scombrus, from the Mediterranean and Black Seas and the NE Atlantic region as far north as the Faeroes. Records from other parts of the world require confirmation. Those from the NW Atlantic (Linton, 1901, 1940; Nahhas & Short, 1965; Nahhas & Powell, 1971) are mainly from stromateid fishes and are based on Distomum gulosum Linton, 1901, which we believe more closely resembles L. cristatum (Rudolphi, 1819) than L. excisum. The records from the Atlantic coast of Africa all lack descrip- tions and in many cases the hosts listed suggest the possibility that other species are involved. Records include Solonchenko (1966, 1968) from Scomber japonicus off Namibia, Fischthal & Thomas (1971) from S. japonicus and several non-scombrid hosts off Ghana, Fischthal & Thomas (19720) from Arnoglossus imperialis off Senegal, and Siddiqi & Hafeezullah (1975) from a stromateid and a polynemid off Nigeria. In 1971 Fischthal & Thomas also described two new species, L. mecoderum and L. unibulbolabrum, from a polynemid and a dactylopterid, respectively, from off Ghana, and in 1980 Fischthal claimed to have found the latter species in S. japonicus in the eastern Mediterranean. In view of this, all of the African records of L. excisum
52
D. I. GIBSON & R. A. BRAY
can at present be considered questionable, and many are perhaps more likely to belong to L. cristatum which occurs in stromateids and Arnoglossus (see below) and closely resembles Fischthal & Thomas' (1971) description of L. unibulbolabrum.
Non- Atlantic records of L. excisum include several Pacific and Indian Ocean reports. Manter (1954) claimed to have found immature specimens in Caesioperca and Paraperca off New Zealand, and Boyle (1966) followed Manter's identification when he reported a metacercaria in Pleurobrachia pileus also in New Zealand waters. In Australian waters Korotaeva (1974) claimed to have found L. excisum in Scomber australasicus and Rastrelliger kanagurta, but gave no description. Our observations of material from the latter host from off Malaya and South Africa suggest that Korotaeva's material may have been one of the Indo-Malaysian species, such as L. angustiovum Yamaguti, 1953. Records from the Gulf of Tonkin and South China Sea (Oshmarin, 1965; Lebedev, 1970; Mamaev, 1970), mainly from carangids, suggest, judging from Oshmarin's brief description, that this material would be better accommodated in one of the very confused Indo-Malaysian species, such as L. megalaspis Yamaguti, 1953 (see Table 7).
More convincing records of L. excisum are those of Layman (1930), Yamaguti (1934), Zhukov (1960), Ichihara et al. (1968), Machida et al. (1970, 1972) and Ichihara (1974), mainly from S. japori&us, but also from a wide range of other hosts, in the Sea of Japan and other Japanese waters. Only Yamaguti (1934), Zhukov (1960) and Ichihara et al. (1968) give descriptions; but none is detailed enough to permit a confident identification, although they do resemble L.
Table 7 The relationship of Lecithocladium spp. of the Indo-Malaysian region
Group Species
Main hosts
Features
L. angustiovum Yamaguti, 1953 Syns:
L. scombri Yamaguti, 1953 L. bulbolabrum Reid, Coil &
Kuntz, 1966
L. unibulbolabrum Fischtal & Thomas of Al-Yamani & Nahhas (1981)
L. apolecti Velasquez, 1962 Syns:
? L. annulatum Chauhan, 1945
L. excisiforme of Gupta & Sehgal (1971)
L. psenopsis Yamaguti of Bilqees(1981)
L. hexavitellarii (Bilqees, 1971)
L. anteporus (Bilqees, 1971)
L. tetravitellarii (Bilqees, 1971)
L. microductus (Bilqees, 1971)
L. arabiana (Bilqees, 1971)
L. octovitellarii (Bilqees, 1971)
L. microcaudum (Bilqees, 1971)
L. stomatei Farooq & Khanum, 1980
L. parviovum Yamaguti, 1953 Syns: ? L. annulatum of Gupta &
Seghal(1970) Cleftocolleta magnum Sahai & Srivastava, 1978
Scombrid genus Rastrelliger
Stromateids, especially Stromateus and Formio niger
Mainly Rastrelliger, carangids and ? stromateids
Up to 4 mm in length; oral sucker much larger than ventral sucker; eggs 16-22 /mi
Up to 14 mm in length; oral sucker much larger than ventral sucker;
Up to 12 mm in length; oral sucker larger than ventral sucker; eggs 13-19//m
HEMIURIDAE
53
Table 7 continued
Group Species
Main hosts
Features
L. ker dense Gupta & Gupta, 1978 L. indicum Gupta & Gupta, 1978 ? L. elongatus Gupta &
Puri, 1982 ? L. srivastavai Gupta &
Puri, 1982 ? L. stromateusi Gupta &
Puri, 1982
? L. sciani Gupta & Puri, 1982 ? L. pampi Lebedev of Gupta &
Puri (1982) ? L.fotedari Gupta & Singh, 1983
D L. megalaspis Yamaguti, 1953 Mainly carangids
Syns: ? L. angustiovum of Fischthal &
Kuntz (1964) L. dawesi Bashirullah &
D'Silva, 1973
L. inglisi Gupta & Ahmad, 1977 L. purense Gupta & Gupta, 1978 ? L. arabicum Farooq &
Khanum, 1980 ? L. singhi Gupta & Singh, 1983
E L. glandulum Chauhan, 1945
Syns:
L. carultum Chauhan, 1945 L. triacantha Gupta &
Gupta, 1978
L. thapari Gupta & Gupta, 1978 ? L. psettodi Gupta & Puri, 1982 ? L. manteri Gupta & Puri, 1982
F L. harpodontis Srivastava, 1937
Syns:
? Clupenurus piscicola
Srivastava, 1935 L. brevicaudum Srivastava, 1937 L. ilishae Mamaev, 1970, nee
Bashirullah & D'Silva, 1973 L. ilishae Bashirullah &
D'Silva, 1973, nee Mamaev, 1970 L. chauhani Hafeezullah, 1975 Colletostomum muthiahi Sahai &
Srivastava, 1978
G L. karachii Zaidi & Khan, 1977 Carangids
Syns:
L. pakistanensis Zaidi &
Khan, 1977
? L. magnetacetabulum Yamaguti of some authors
Variety of hosts, especially sciaenids
Variety of hosts, including the clupeid Hilsa
Up to 4 mm in length; suckers similar in size; eggs 16-26^m (usually 20-24 //m)
Up to 6 mm in length; suckers similar in size or ventral sucker slightly larger; eggs 20-23 fan
Up to 6 mm in length; suckers similar in size or ventral sucker slightly larger; eggs 12-20 /an
Up to 5 mm in length; ventral sucker much larger than oral sucker; eggs 1 5-20 /an
54 D. I. GIBSON & R. A. BRAY
excisum. The records from S. japonicus suggest that the identifications may be reliable, especially as the latitude of their recovery is similar to that of the NE Atlantic. The presence of L. excisum in this region does, however, require confirmation.
Zhukov (1977) maintained that several species of Lecithocladium from the Indian coast, described by Srivastava (1937, 1942) and Chauhan (1945), are synonyms of L. excisum. The Indo-Malaysian region contains numerous nominal Lecithocladium species, many poorly described and all in a state of confusion. A study of the literature has revealed that little account has been taken of intra-specific variation, fixation artifacts or functional variation in the erection of these numerous taxa. In Table 7 we have attempted to bring some semblance of order by reducing the more than forty nominal species to only six, and some of the latter are very similar to each other. We hope that this drastic action will, at least, provoke further critical investigation and make at least some sort of reasonable identification of Indo-Malaysian forms possible. The most similar species to L. excisum in Table 7 are L. angustiovum Yamaguti, 1953 and L. parviovum Yamaguti, 1953. Specimens in the Collection of the BM(NH) identified as L. angustiovum from Rastrelliger kanagurta off Pinang, Malaysia, can be distinguished from L. excisum by their much smaller size. L. parviovum differs from L. excisum in its markedly smaller eggs. As indicated in Table 7, we are doubtful whether L. excisum occurs in the Indian Ocean.
Several authors (Dawes, 1947; Nahhas & Short, 1965; Fischthal & Thomas, 1971; Zhukov, 1977) list L. cristatum as a synonym of L. excisum, despite Looss' (1908) clear descriptions. We regard L. cristatum as distinct for the reasons given by Gibson (1976), and, incidentally, doubt the validity of L. falklandicum Gaevskaja & Kovaleva, 1978, a new name for L. cristatum of Gibson (1976). L. cristatum has not been recorded in the NE Atlantic; but, as it is known to occur in stromateids, it may be present in Stromateus fiatola in the south of the region. It is worth noting that in the Collection of the BM(NH) there are specimens which, in possessing a distinct 'Nacken-buckel', are clearly identifiable as L. cristatum. They are believed to have come from a species of Arnoglossus in the Mediterranean Sea. Fischthal & Thomas (1972a) recorded 'L. excisum' from Arnoglossus off Senegal, and, from another west African locality, Ghana, these authors (1971) described a species, L. unibulbolabrum, possessing a 'Nacken-buckel' and closely resembling L. cristatum. As mentioned above, Fischthal (1980) recorded L. unibulbolabrum from several hosts in the Mediterranean Sea, so it seems likely that this species can be considered a synonym of L. cristatum. Consequently, bearing in mind our earlier comments on D. gulosum, it would appear that L. cristatum has a much wider distribution than previously believed. L. mecoderum Fischthal & Thomas, 1971, may also be a synonym of L. cristatum.
We have included L. crenatum (Molin, 1859) as a questionable synonym of L. excisum, although Looss (1908) considered that it was possibly a valid species. Molin (1859) described it from Centrolophus niger at Padua, Italy, claiming to have found over 100 specimens. Apart from nine specimens reported by Looss (1908) from Trieste, Italy, there are no further records of Lecithocladium spp. from this host. Molin's figure resembles L. excisum, although the host (a stromateoid) and Looss' comments suggest the possibility of a closer relationship with L. cristatum. We have recovered some poorly preserved and contracted specimens of Lecithocladium from a specimen of C. niger from Bordighera, Italy, now housed in the Fish Collection of the BM(NH). In having the oral sucker significantly larger than the ventral and in having eggs of 20-25 urn in length, these worms resemble L. excisum, and are herein considered to indicate that L. crenatum, although found on the other side of Italy, is possibly a synonym of L. excisum.
The distribution of L. excisum can, therefore, be definitely stated as including the Mediterranean and Black Seas and the NE Atlantic region. Whether or not it occurs in Japanese waters needs further investigation; but it seems unlikely that it is the widespread species which an uncritical examination of the literature would suggest.
Subfamily GLOMERICIRRINAE Yamaguti, 1958
DIAGNOSTIC FEATURES. Ecsoma well developed. Body-surface plicated. Pre-somatic pit absent. Testes oblique to tandem. Seminal vesicle bipartite; both parts globular to spindle-shaped; anterior part muscular; in hindbody or dorsal to ventral sucker. Pars prostatica tubular; short;
HEMIURIDAE 55
linked to seminal vesicle by aglandular duct. Oval sinus-sac present; in hindbody, dorsal to ventral sucker or occasionally in forebody ; enclosing glandular ejaculatory vesicle. Hermaphroditic duct convoluted. Sinus-organ present; amuscular; long; convoluted. Genital atrium well developed; long and wide proximally. Vitellarium two irregularly oval to indistinctly lobed, symmetrical masses. Excretory arms united in forebody. Parasitic in stomach of marine teleosts.
Genus GLOMERICIRRUS Yamaguti, 1937 DIAGNOSTIC FEATURES. As subfamily. TYPE SPECIES. Glomericirrus amadai Yamaguti, 1937 [by original designation].
Glomericirrus macrouri (Gaevskaja, 1975) Gaevskaja, 1979
'Genus novum D, species nova' of Armstrong (1974). Hemiurus macrouri Gaevskaja, 1975. ? Dinosoma sp. of Zubchenko (1975). Glomericirrus n. sp. of Haedrich & Polloni (1976). Glomericirrus ulmeri Campbell & Munroe, 1977.
TYPE-HOST AND LOCALITY. Coryphaenoides rupestris, northern North Mid-Atlantic Ridge. RECORDS
(i) Material studied (a) From the NE Atlantic
Coryphaenoides rupestris [stomach] W of the Faeroes (62°N, 1 1°W; depth 820-860 m; June, 1974). BM(NH) 1983.12.12.1-2.
[stomach] SW of Rockall (56°N, 17°W; depth 640m; June, 1974). BM(NH) 1983.12.13.3^.
- [stomach] Off St. Kilda (58°N, 10°W; depth 820-825 m; Oct., 1978) BM(NH) 1983.12.13.5; (depth 990-1000 m; Oct., 1978) BM(NH) 1983.12.13.6.
[stomach] Off Flannan Island, W Scotland (59°N, 08°W; depth 900-920 m; Oct., 1978). BM(NH)
1983.12.13.7. Hoplostethus atlanticus [stomach] Rosemary Bank, W of Scotland (59°N, 11°W; depth 970-1025 m; June
1974). BM(NH) 1983.12.13.8. Nezumia aequalis [stomach] Off Tory Island, NW Ireland (55°N, 10°W; depth 880-1000 m; June, 1974).
BM(NH) 1983.12.13.9. Trachyrincus trachyrincus [stomach] WNW Sulisker (Sula Sgeir), NW Scotland (59°N, 08°W; depth
11 20-1 140m; Apr., 1973). BM(NH) 1983.12.13.10.
- [stomach] Off St. Kilda (58°N, 10°W; depth 1300-1320 m; Oct., 1978). BM(NH) 1983.12.13.11.
(b) From elsewhere None.
(ii) NE Atlantic records from the literature
Coryphaenoides rupestris [stomach] Northern North Atlantic Ridge. Gaevskaja (1975: 458; as Hemiurus macrouri; 1979: 269); Zubchenko (198 la: 28).
(?) [stomach] North Atlantic. Zubchenko (1975: 235; as Dinosoma sp.).
(?) Macrourus berglax [stomach] North Atlantic, Zubchenko (1975: 235; as Dinosoma sp.).
ASPECTS OF BIOLOGY. Virtually nothing is known about the biology of this species. For the present we are restricting our concept of the species to forms from macrourids and neighbouring deep- water fishes, although it is possible that future work may show that it also occurs in some coastal flatfishes. Definite records of this species indicate that it occurs in a wide range of macrourids on both sides of the North Atlantic on the edge of the continental shelf and on the Northern Mid- Atlantic Ridge at depths of mainly between 500 and 2000 metres, although it is possible that Campbell & Munroe (1977) obtained material from below these depths. On the western side of the North Atlantic (see Armstrong, 1974; Campbell & Munroe, 1977; Campbell et al., 1980; Zubchenko, 19816; Campbell, 1983) its range extends into the Gulf of Mexico. In addition, it has also been recorded in the South Atlantic in the region of the Falkland Isles (Gaevskaja & Rodjuk, 1983), in the sub-Antarctic region (Rodjuk, 1981) and off Angola and Namibia (Gaevskaja &
56 D. I. GIBSON & R. A. BRAY
Aleshkina, 1983). Whether or not it occurs off Japan requires further study (see below). In addition to macrourids, we have also found it in the trachichthyid fish Hoplostethus atlanticus, which until recently was virtually unknown in the NE Atlantic. This fish is now known to occur in relatively large numbers in the same bathyal habitat as the macrourids on the edge of the continental shelf as far north as Flannan Island off the NW coast of Scotland (Bridger, 1978; as Gephyroberyx darwini: see Merrett & Wheeler, 1983).
PREVIOUS DESCRIPTIONS. Armstrong (1974: 142; as 'Genus novum D, species nova'); Gaevskaja (1975: 458; as Hemiurus macrouri; 1979: 269; terminal genitalia only); Campbell & Munroe (1977: 285; as G. ulmeri).
DESCRIPTION (Fig. 1 1). The body of this relatively small worm is fusiform; but widest at the level of the ventral sucker, which protrudes considerably, making it difficult to mount specimens dorso-ventrally, and at the level of the vitellarium (Fig. 1 1A). The ecsoma may be withdrawn or extend up to about half the length of the soma (or to as long as the soma according to Gaevskaja, 1975). It is most usually withdrawn in poorly preserved material. Most of the body-surface, with the exception of the ecsoma, is covered with annular plications. These reach posteriorly to a level just anterior to the posterior extremity of the soma in the ventral field, to about the level of the vitellarium in the lateral fields and to about the level of the testes in the dorsal field. In addition, plications are absent or reduced to minute corrugations mid-ventrally in the forebody. The plications are slightly crenulate, often more distinctly so than in Brachyphallus crenatus, but normally less so than in Dinosoma spp. The oral sucker is ventrally subterminal and surmounted by an insignificant pre-oral lobe. The forebody is short, conical and concave ventrally. The ventral sucker is very large, the sucker-ratio being within the range of 1 : 2-3. It is round, protrudes significantly and the lumen tends to be oriented antero-ventrally (Fig. 11 A). The measurements of this species are given in Table 8.
There is no prepharynx, the oral sucker opening directly into a muscular, oval pharynx. This in turn opens posteriorly in our sectioned material into a short, muscular oesophagus, which almost immediately bifurcates to form two short, postero-laterally oriented ducts that open into a small pair of 'Driisenmagen', each with a muscular wall and a coarse, villous lining. These in turn open into the caeca-proper which extend posteriorly in the dorso-lateral field and terminate blindly normally within the ecsoma and occasionally close to its posterior extremity. One caecum may extend considerably further posteriorly than the other.
The excretory pore is situated ventro-terminally on the ecsoma. This opens into a short section of the excretory vesicle of variable width (but often very dilate), which extends about one-quarter of the length of a well-protruded ecsoma. This is very similar to the situation in Brachyphallus crenatus, except that this region has no distinct villous lining. It is separated from the rest of the stem of the vesicle by a distinct valve. The narrow stem continues forward mid-ventrally into the soma and then passes antero-dorsally past the ovarian complex into the mid-dorsal field at the level of the posterior testis. In our sectioned material, the vesicle bifurcates at this level and the two, narrow arms run forward ventro-laterally to pass on either side of the seminal vesicle. The arms continue into the forebody in the lateral fields and unite dorsally to the pharynx.
The two subglobular testes occur obliquely and contiguously or close together roughly half- way between the ventral sucker and the ovary, although their position and size are variable. The posterior testis tends to be on the same side of the body as the ovary, and both testes tend to occur in the ventro-lateral fields, although one is often more dorsal than the other. Occasionally, the testes occur almost in tandem. The short vasa efferentia leave the testes antero-dorsally and, in our sectioned specimens, pass dorsally to enter the seminal vesicle. Although they appear to unite as they pass into the wall of the seminal vesicle, this union is not clear in our sections. The seminal vesicle is bipartite. The two parts are variable in size, depending upon the amount of spermatozoa that they contain, and are frequently larger than the testes. Although the proximal part is usually the smaller, this is not always so. Both parts tend to be oval, but the proximal part has a thin wall, while the distal part is characterized by having a very thick, muscular wall similar to that of the seminal vesicle of elytrophalline hemiurids (Fig. 1 IB). The narrow union between
HEMIURIDAE
57
B
Fig. 11 Glomericirrus macrouri. (A) Entire worm, ex Trachyrincus trachyr incus; (B) Sagittal section of anterior half of worm, ex Coryphaenoides rupestris. Scale bars: A 500 //m; B 200 //m.
58 D. I. GIBSON & R. A. BRAY
Table 8 Measurements of Glomericirrus macrouri
|
Authority |
Armstrong (1974) |
Gaevskaja(1975) |
Campbell & |
Present material |
|
Munroe (1977) |
||||
|
Name used |
Genus novum D, |
Hemiurus |
Glomericirrus |
Glomericirrus |
|
species nova |
macrouri |
ulmeri |
macrouri |
|
|
Host |
Macrourids |
Coryphaenoides |
Coryphaenoides |
Coryphaenoides |
|
rupestris |
spp. |
rupestris etc. |
||
|
Locality |
Gulf of Mexico, |
North Mid- |
Hudson Canyon, |
NE Atlantic |
|
Caribbean |
Atlantic Ridge |
NW Atlantic |
||
|
Length (mm) |
1-9-2-9 |
2-79 |
1-7-3-1 |
1-35-2-15 |
|
Breadth (mm) |
0-6-0-87 |
0-68 |
0-39-0-6 |
0-22-0-42 |
|
Ecsoma (mm) |
0-42-0-89 |
1-43 |
0-45-0-82 |
0-0-82 |
|
Forebody (mm) |
0-2-0-43 |
- |
- |
0-12-0-21 |
|
Oral sucker (mm) |
0-08-0- 12 x |
0-1x0-12 |
0-1-0-13 x |
0-09-0- 12 x |
|
0-09-0-12 |
0-09-0-12 |
0-09-0-11 |
||
|
Ventral sucker |
0-21-0-31 x |
0-31x0-35 |
0-25-0-35 x |
0-2-0-31 x |
|
(mm) |
0-23-0-26 |
0-23-0-25 |
0-21-0-3 |
|
|
Sucker-ratio |
1 : 2-05-2-54 |
1:3 |
1:2-2-3-1 |
1 : 2-2-2-57 |
|
Testes (mm) |
0-06-0-22 x |
0-09-0-2 x |
0-1 1-0-27 x |
0-05-0- 13 x |
|
0-15-0-27 |
0-15-0-23 |
0-07-0-18 |
0-07-0-18 |
|
|
Ovary (mm) |
0-12-0-21 x |
0-15x0-26 |
0-08-0-21 x |
0-08-0- 14 x |
|
0-18-0-28 |
0-15-0-3 |
0-09-0-19 |
||
|
Vitelline masses |
0-1 1-0-22 x |
0-2x0-15-0-26 |
0-12-0-31 x |
0-12-0- 16 x |
|
(mm) |
0-14-0-23 |
0-11-0-23 |
0-12-0-21 |
|
|
Eggs (/zm) |
21-27x13-16 |
23x14 |
19-24x12-14 |
22-26 x 1 1-14 |
the two parts is surrounded by a sphincter. The seminal vesicle occurs between the testes and the ventral sucker, but is usually closer to the testes, and often extends dorsally or dorso-laterally to the anterior testis. Anteriorly the muscular, distal part gives rise to a narrow, aglandular duct, which may be convoluted or straight, depending upon how close the seminal vesicle is to the base of the sinus-sac. In our sectioned material the duct is relatively short and convoluted. It leads to the base of the sinus-sac and passes through the wall of this organ. In our sectioned material there is no clear evidence, such as the nature of the lining of the duct, which indicates that it is or becomes the pars prostatica (cf. Campbell & Munroe, 1977). There are a number of external prostatic gland-cells, but they appear to surround only the distal end of this duct (Fig. 1 IB). As it passes through the wall of the sinus-sac, the wall of the duct appears to become wider and more glandular: this very short region may well be the pars prostatica (sensu s trie to). Within the sinus-sac this opens into a very distinct glandular ejaculatory vesicle (terminology of Gibson & Bray, 1979). In our sections there is no evidence that the external prostatic cells surrounding the base of the sinus-sac pass through the wall of the sinus-sac and open into this organ. It seems likely, therefore, that the pars prostatica is a very reduced structure, as it is in several of the lecithochiriines where a glandular ejaculatory vesicle occurs. The lumen of the ejaculatory vesicle is almost filled with large, anucleate cells or blebs typical of the glandular form of this organ. The sinus-sac itself is large, oval and sunk deep within the body. It is usually situated in the anterior hindbody or postero-dorsally to the ventral sucker; but, although this was not seen in our material, it may apparently occur antero-dorsally to this sucker, its position depending upon the state of eversion of the sinus-organ, the state of contraction of the body and the amount of pressure applied to the specimen during fixation and mounting. The terminal portion of the uterus enters the base of the sinus-sac just antero-ventrally to the male duct and passes over the ventral surface of the ejaculatory vesicle (Fig. 11B). It widens as it passes anteriorly and the ejaculatory vesicle opens into it distally via a sphincter to form an hermaphroditic duct. This is
HEMIURIDAE 59
usually a very convoluted structure, but the amount of convolution is reduced when the sinus- organ is greatly everted. Dorsally to the ventral sucker or slightly anterior or posteriorly to this, depending upon its position, the sinus-sac joins the very deep genital atrium. The latter may be cylindrical or taper anteriorly, depending upon the amount of convolution of the sinus-organ. At the junction of the sinus-sac and the genital atrium the hermaphroditic duct passes into a large, permanent, relatively amuscular and often convoluted sinus-organ. This organ may end within the genital atrium or protrude through the genital pore (in specimens of G. thoria we have seen it protrude up to one- third the length of the body). The genital pore occurs mid-ventrally, roughly at the level of the junction between the oral sucker and the pharynx. In several of the specimens, including the sectioned material, the distal portion of the genital atrium, roughly equivalent in length to the pharynx, is slightly narrower and has a thicker lining and a more muscular wall: when withdrawn the sinus-organ usually terminates immediately behind this region (Fig. 1 IB).
The transversely oval ovary occurs subventrally on either side of the worm within about the middle third of the hindbody, although in extremely extended or contracted forms it may be posterior or anterior to this region, respectively. The oviduct leaves the ovary posteriorly and receives the duct from Juel's organ. It then continues postero-laterally over the lateral surface of Mehlis' gland, and, immediately prior to entering Mehlis' gland postero-laterally, it receives the vitelline ducts, apparently together. Within Mehlis' gland the oviduct swells slightly to form what is probably the ootype and then passes anteriorly. Mehlis' gland is situated posteriorly to the ovary and antero-dorsally to the vitellarium. Juel's organ is large and situated dorsally or antero- dorsally to Mehlis' gland. The uterus leaves Mehlis' gland anteriorly and immediately loops back over the dorsal surface of this organ, its initial loops being surrounded by small gland-cells. Posterior to Mehlis' gland it widens to form a uterine seminal receptacle. The latter is often a very large structure with spermatozoa filling much of the uterus posterior to the vitellarium. The uterine coils descend on the ovarian side of the body, usually reaching into the ecsoma, although not normally as far as the caeca. They then ascend on the opposite side of the body. The distri- bution of the uterus anteriorly to the ovary is variable, depending upon the displacement of the testes and the seminal vesicle; but usually, at the level of the anterior margin of the ovary, the uterus extends across the body ventrally and normally fills the space between the ovary and the posterior testis (Fig. 1 1 A). It then passes dorsally to the testes, occasionally looping ventrally to the posterior testis, and then coils ventrally or ventro-laterally to the seminal vesicle, prior to passing dorsally and narrowing considerably to enter the base of the sinus-sac. There is no obvious delineation of a metraterm. The uterus contains numerous small, operculate eggs. The vitellarium is composed of two indistinctly lobed masses, which occur slightly obliquely immedi- ately posterior to the ovary, the anterior of the two masses being more medially positioned and the other being more directly posterior to the ovary. If lobation is distinguishable on masses, then it normally occurs as four lobes on one mass and three on the other. The lateral collecting ducts leave the masses dorso-medially and appear to unite as they join the oviduct. In our sections there is no obvious common duct.
DISCUSSION. The genus Glomericirrus was erected by Yamaguti (1937) for a new species, G. amadai, a single specimen of which he found in the stomach of the branchiostegid fish Branchiostegus japonicus off Japan. He later (1938) redescribed this species from further specimens recorded from B. japonicus, Argentina kagoshimae, Cepola schlegeli and Lotella phycis. We have examined the holotype, and, although it is very darkly stained and heavily flattened, we consider it to be very similar to our material from macrourids in the NE Atlantic, differing significantly only in the sucker-ratio (see Table 8), which is less than 1 : 2. More recent records of G. amadai by Machida et al. (1970) and Ichihara (1974) from Aulopus japonicus and Percanthias japonicus off the Tsushima Isles, Sea of Japan, by Korotaeva (1970) from Nemadactylus valenciennes and by Korotaeva (1982) from Cyttoidops mccullochi, both from Australian waters, do not include descriptions. It is, however, worth noting that we have been informed by Dr Ichihara (in lift.) that his specimens had a sucker-ratio of 1 : 2-2. It is clear that further work must be carried out on Japanese material; but, at present, the significant host and geographical disparity makes it more prudent to consider our material distinct from G. amadai.
60 D. I. GIBSON & R. A. BRAY
G. propositus was originally described from two specimens taken from the macrourid Coryphaenoides garmani off Japan by Yamaguti (1938). There appears to be no further records of this name in the literature. We have examined Yamaguti's holotype and consider that it is very similar to the present material from macrourids of the north-east Atlantic, except for a marginal difference in egg-size and the position of the sinus-sac. Yamaguti gives the egg-length as being 24-33 /mi, but we made the range in eggs from the distal region of the uterus in the holotype to be 24-29 /mi, with the majority being about 26-27 /mi, and thus marginally larger than in forms from the Atlantic (see Table 8). With regard to the position of the sinus-sac, a close examination of the type-specimen clearly shows that it has been heavily flattened and the alignment of the crenulate plications suggests that the ventral sucker has been pushed back during the flattening process. Thus the sinus-sac could have been forced forward. Although the sinus-sac is postero- dorsal or posterior to the ventral sucker in our acetic-acid-fixed material, Armstrong (1974) noted its position as 'dorsal to acetabulum (occasionally antero-dorsal, rarely postero-dorsal to acetabulum)'. Furthermore, we have some poorly fixed material of Glomericirrus (see below) from Arnoglossus sp. (probably from the Gulf of Guinea) in which the sinus-sac ranges from antero-dorsal to posterior to the ventral sucker. The position of this organ is, therefore, probably variable, depending upon the contraction of the body, the contraction of the genital atrium, the method of fixation and the degree of flattening during fixation. However, because (1) we cannot be certain the position of the sinus-sac in Yamaguti's material is not normal, and because of (2) the slight difference in egg-size and (3) the geographical separation between these forms, we have refrained from calling our specimens G. propositus. Nevertheless, it is possible that further material from Japanese waters may prove the two forms to be conspecific.
In 1966 Nikolaeva described Dinosoma thoria from a single specimen taken from Arnoglossus thori in the Aegean Sea (although this species of fish is not supposed to extend as far east as the Aegean: Hureau & Monod, 1973; Wheeler, 1978). We agree with Toman (1973), who suggested that this species rightfully belongs to Glomericirrus. The specimens mentioned above from Arnoglossus sp. probably from the Gulf of Guinea (the exact locality data have been lost) appear to be specimens of G. thoria n. comb. Furthermore, we could find no distinct morphological difference between these specimens and those from macrourids in the NE Atlantic, although the former specimens are not in as good a state of preservation as the latter. For the present we have retained G. thoria as a species distinct from the form from macrourids mainly because it is diffi- cult to rationalize the totally different habitats of the two host-groups, one form occurring in coastal flatfishes and the other in bathyal macrourids (and a trachichthyid). The question of the synonymy of G. thoria and the species from macrourids can only be solved by the examination of well-preserved specimens from Arnoglossus and by an understanding of the life-history of these worms.
The first named material which we can be reasonably certain is identical to our material from macrourids is that described by Gaevskaja (1975) as Hemiurus macrouri from Coryphaenoides rupestris on the northern part of the Northern Mid- Atlantic Ridge. Gaevskaja (1978 in litt.) agreed with us that this was in fact a species of Glomericirrus, and she later (1979) transferred it to this genus and listed G. ulmeri Campbell & Munroe, 1977, as a synonym. The latter species, originally mentioned by Haedrich & Polloni (1976) as 'Glomericirrus n. sp.', was recorded from Coryphaenoides carapinus, C. leptolepis and C. armatus from the Hudson Submarine Canyon on the edge of the continental shelf on the western side of the northern North Atlantic. Campbell et al. (1980) added C. rupestris to the list of hosts from the same region. Specimens from the western side of the North Atlantic had in fact been described earlier as 'Genus novum D, species nova' by Armstrong (1974), who recorded them from six species of the macrourid genera Coelorhynchus, Hymenocephalus , Ventrifossa and Nezumia in the eastern Gulf of Mexico off Florida (depth 364-728 m) and in the Caribbean Sea off Panama (depth 591 m). It had also been found in the NW North Atlantic by Zubchenko (1976; as Hemiurus macrouri; 1981a,£) in Coryphaenoides rupestris and Nezumia bairdi. We agree with Gaevskaja (1979), Campbell (1983), Gaevskaja & Aleshkina (1983) and Gaevskaja & Rodjuk (1983) that G. ulmeri is a synonym of G. macrouri. In conclusion, therefore, we have used the name G. macrouri for our material and note that Trachyrincus trachyrincus and Hoplostethus atlanticus are new host-records.
HEMIURIDAE 61
The following points are also worth noting. (1) Due to the fact that the tegumental plications of Glomericirrus spp. are crenulate, there has been confusion between this genus and Dinosoma Manter, 1934 (e.g. Nikolaeva, 1966). It is possible, therefore, that this may also be the case with Dinosoma sp. from the trachichthyid Gephyroberyx japonicus which Ichihara et al. (1965) reported off Japan, although as shown below, Dinosoma can occur in bathyal fishes. (2) As indicated by Manter (1970), Glomericirrus septemlobus Freitas & Kohn, 1965, is a lecithochiriine and probably a synonym of Lecithochirium microstomum Chandler, 1935. (3) Despite the fact that Szuks (1980) examined large numbers of Coryphaenoides rupestris in the Labrador Sea, surpris- ingly he did not record G. macrouri: he did, however, claim to have found the warm-water species Parahemiums merus (see p. 38)! (4) We have elucidated, for the first time (Fig. 1 IB), exactly where the sinus-sac and the genital atrium unite and can thus present a much more accurate picture of the shape of the sinus-sac and the functioning of the terminal genitalia of this subfamily.
Subfamily LECITHOCHIRIINAE Lime, 1901
Sterrhurinae Looss, 1907.
Brachyphallinae Skrjabin & Guschanskaja, 1955.
Tricotyledoniinae Skrjabin & Guschanskaja, 1955.
Trithelaminae Yeh, 1955.
Dissosaccinae Yamaguti, 1958.
DIAGNOSTIC FEATURES. Ecsoma usually well developed, occasionally reduced. Body-surface usually smooth, but occasionally plicated or rugate. Muscular 'shoulder-pads' present or absent. Presomatic pit and ventro-cervical groove present or absent. Testes tandem to symmetrical, usually oblique. Seminal vesicle elongate; constricted into two portions, which are occasionally separated by a duct, or tubular and convoluted; in bipartite forms anterior half may have thicker wall; normally in forebody, but forms with halves separated by duct may extend into hindbody. Pars prostatica short; vesicular or tubular; may extend slightly into base of sinus-sac; linked to seminal vesicle by short, aglandular duct. Sinus-sac present; rarely of 'open'-type; enclosing distinct ejaculatory (prostatic) vesicle and metraterm (or part of metraterm). Permanent sinus- organ absent. Genital atrium usually small or absent, occasionally well developed. Uterus mainly pre-ovarian or roughly equally distributed in pre- and post-ovarian fields. Eggs without filaments. Vitellarium seven digitiform to oval lobes in lateral groups of three and four, or with tendency to become two distinct lateral masses which often exhibit three and four lobes. Excretory arms united in forebody. Normally parasitic in gut or body-cavity of marine teleosts.
Key to the lecithochiriine genera occurring in the north-east Atlantic
1 Vitellarium seven distinct oval to digitiform lobes which may occur as two 3- and 4-lobed masses;
body surface smooth Lecithochirium (p. 61)
Vitellarium two entire masses which may be indistinctly 3- and 4-lobed; body surface with plications Brachyphallus (p. 90)
Genus LECITHOCHIRIUM L\ihe, 1901
Sterrhurus Looss, 1907.
Ceratotrema Jones, 1933.
Jajonetta Jones, 1933.
Separogermiductus Skrjabin & Guschanskaja, 1955.
Magniscyphus Reid, Coil & Kuntz, 1965.
Neohysterolecitha Ahmad, 1977.
DIAGNOSTIC FEATURES. Ecsoma well or poorly developed. Body-surface smooth. Pre-oral lobe rarely with two lateral knobs ('horns'). Presomatic pit and/or ventro-cervical groove often present. Seminal vesicle bipartite, apparently tripartite or occasionally coiled; in forebody. Pars prostatica tubular, with wide lumen, to vesicular. Short, narrow extension of pars prostatica
62 D. I. GIBSON & R. A. BRAY
and/or ejaculatory duct may be present within sinus-sac. Ejaculatory (prostatic) vesicle linked posteriorly to antero-dorsally with pars prostatica or ejaculatory duct. Temporary sinus-organ may form. Vitellarium two lateral masses; usually divided into three and four oval to digitiform lobes. Parasitic in gut (mainly stomach) or body-cavity of marine teleosts; also recorded from hepatic ducts and gills of marine teleosts and (?) gut of freshwater reptiles.
TYPE-SPECIES. Lecithochirium rufoviride (Rudolphi, 1819) [by original designation]. COMMENT. The systematics of this genus was discussed by Gibson & Bray (1979).
Key to the species of Lecithochirium recorded from the north-east Atlantic
1 Oral sucker with postero-lateral thickenings of wall which protrude into lumen of sucker . . 2 Oral sucker without postero-lateral thickenings of wall 3
2 Two symmetrical, lateral projections ('horns') present on pre-oral lobe; parasitic in body-cavity
of rockling or occasionally stomach of eels L.furcolabiatwn(p.69)
No projections present on pre-oral lobe; normally parasitic in stomach of eels .... L. rufoviride (p. 62)
3 Vitellarium with seven digitiform lobes often arranged in rosette; normally parasitic in stomach
of conger eels L.fusiforme(p.76)
Vitellarium composed of two 3- and 4-lobed masses; parasitic in stomach of wide range of teleosts and body-cavity of rock-pool fishes, especially gobiids . . L. musculus (p. 83)
Lecithochirium rufoviride (Rudolphi, 1819) Liihe, 1901
Distoma rufoviride Rudolphi, 1819.
Distoma (Apoblema) rufoviride (Rudolphi) Dujardin, 1845.
Apoblema rufoviride (Rudolphi) Juel, 1889.
Hemiurus rufoviridis (Rudolphi) Looss, 1899.
(?) Distoma grandiporum Rudolphi of Olsson (1876).
(?) Cercaria vaullegeardiPelseneer, 1906.
Distomum ocreatum Molin of Johnstone (1907).
Lecithochirium gravidum Looss, 1907.
Dissosaccus gravidus (Looss) Skrjabin & Guschanskaja, 1955.
TYPE-HOST AND LOCALITY. Conger conger, Naples, Italy. RECORDS
(i) Material studied
(a) From the NE Atlantic
From the gut
Anguilla anguilla [stomach] Kristineberg, Sweden (Aug., 1976). BM(NH) 1984.9.19.1-12. Conger conger [stomach] Moray Firth, Scotland (58°N, 02°W; depth 188m, 152-1 86m and 160-1 92m; Sept., 1976). BM(NH) 1984.9.19.13-82.
- [?] Locality unknown. BM(NH) 84.9.20.4-12.
- [stomach] Plymouth, Devon, England. (May) BM(NH) 1932.1 1.29.1 1-21 (Material of Baylis & Jones, 1933; 631; Baylis, 1939: 478); material collected by M. Rothschild - BM(NH) 1932.11.22.56; material collected by J. S. Steward - BM(NH) 1938.11.4.228-240; (May, 1972) BM(NH) 1984.9.19.83-87.
- [?] Guernsey, Channel Islands. Collected by R. H. Le Pelley. BM(NH) 1924.3.15.33-52.
- [stomach] Irish Sea. Collected by F. G. Rees. BM(NH) 1976.4.9.1 14.
— [?] Langesund, Norway (Jan., 1888). Zoological Museum Oslo Reg. No. C. 60.
- [stomach] Barra Bank, off W Scotland (57°N, 09°W; depth 450 m; Oct., 1978). BM(NH) 1984.9.19.88.
- [gut] Locality unknown. Collection of J. Mahon. BM(NH) 1980.7.25.40-^1. [stomach] N. of Scotland (59°N, 02°W; depth 79 m; May, 1984). BM(NH) 1984.9.19.89.
Lophius piscatorius [stomach] Plymouth, Devon, England. Collected by M. Rothschild. BM(NH)
1932.11.22.53-55. (?) Molva molva [stomach] Kristineberg, Sweden (Aug., 1976). BM(NH) 1984.9.19.90.
Encapsulated on viscera (?) Gadus morhua [pyloric caeca] Faeroes. Collected by M. K0ie. BM(NH) 1984.9.19.91.
HEMIURIDAE 63
(b) From elsewhere None.
(ii) NE Atlantic records from the literature
From the gut Anguilla anguilla [stomach] Varberg, Sweden (July). Olsson (1868: 49; as Distoma rufoviride).
[stomach and branchial cavity] Bergen, Norway. (Aug.) Olsson (1868: 49; as D. rufoviride). [?] (July,
Aug.) Lonnberg (1890: 44; as D. rufoviride).
- [stomach] Grafverna and Naset, Bahusiae (Bohuslan), Sweden (July-Sept.). Olsson (1876: 20; as D. rufoviride).
- [?] Kristineberg, Sweden. (Summer, 1889) Juel (1889: 8; as Apoblema rufoviride); Lonnberg (1889: 62; as D. rufoviride); Looss (1908: 149; as Lecithochirium gravidum).
[stomach] St. Andrews, Scotland. Nicoll (1907: 72).
- [stomach] Plymouth, Devon, England. Nicoll (1914: 485).
[stomach] Milford Haven, Dyfed, Wales. Mhaisen (1977; 1983: 345; as L. gravidum).
Conger conger [stomach] (Rennes), Brittany, France. Dujardin (1845: 421: as D. rufoviride: see Dollfus,
1968: 145).
— [stomach] Ireland. Bellingham (1844: 425; as D. rufoviride).
[mouth, stomach] Belgium, van Beneden (1871: 82; as D. rufoviride).
[stomach, intestine] 0resund, Sweden (March). Olsson ( 1 876: 20; as D. rufoviride and (?) D. grandiporum).
- [stomach] Irish Sea. Herdman (1904: 39; as Distomum rufoviride); Johnstone (1907: 277; as D.
ocreatum; see Bruce et al, 1963: 76); Rees & Llewellyn (1941: 391, 393). [stomach] Millport, Firth of Clyde, Scotland. Elmhirst & Martin (1910: 477); Nicoll (1910: 349, 357);
D. O. Jones (1943: 47).
[stomach] Aberdeen, Scotland (Sept., 1908). Nicoll (1913: 193).
[stomach] Plymouth, Devon, England. Nicoll (1914: 485); Baylis & Jones (1933: 631); Baylis (1939:
478); Dawes (1947: 287); Bray (1973: 178); (Sept., Nov.) Matthews (19826: 24).
[stomach] Guernsey, Channel Isles (July). Baylis (1928: 332); Bray (1973: 178).
[stomach] Galway, Eire. Little (1929: 25).
- [stomach] Roscoff, Finistere, France (June, 1937). Sproston (1939: 45, 50). [stomach] Irish Atlantic Slope (54°N, 12°W; depth 220-275 m; Aug., 1939). Rees & Llewellyn (1941:
391, 393).
— [stomach] Milford Haven, Dyfed, Wales. D. O. Jones (1943: 47).
[?] Albufeira, Algarve coast, Portugal (Aug., 1954). Tendeiro & Valdez (19556: 100).
[?] Sines, Baixo Alentejo coast, Portugal. Tendeiro & Valdez (19556: 100).
[?] North Sea off Netherlands. Willemse (1968: 85).
Lophius piscatorius [stomach] Plymouth, Devon, England. Nicoll (1914: 485); Baylis & Jones (1933: 631);
Baylis (1939: 478); Dawes (1947: 287); (June) Matthews (19826; appendix).
— [?] NE Atlantic. Gaevskaja (1978a: 83; possibly not an original record). (?) Osmerus eperlanus [intestine] Belgium, van Beneden (1871: 70; as Distoma rufoviride). (?) Scophthalmus rhombus [stomach, intestine] Belgium, van Beneden (1871: 74; as D. rufoviride). (?) Zoarces viviparus [mouth] Belgium, van Beneden (1871: 49; as D. rufoviride).
Encapsulated on viscera
Those records close to the SW British Isles must be treated as questionable, as some could be L. furcolabiatum (see also L. furcolabiatum and Synaptobothrium caudiporum for other questionable records, some of which might be L. rufoviride). (?) Blennius pholis [intestine, viscera] Roscoff, Finistere, France (June, 1937). Sproston (1939: 40; as L.
gravidum). [liver, occasionally free in gut] Aberystwyth and Milford Haven, Wales. Mhaisen, in Popiel (1978: 155;
as L. gravidum); Mhaisen (1977 and 1983: 345; as L. gravidum). (?) Psetta maxima [visceral cavity] Fish from North Wales reared at Moidart, Scotland. DAFS (1974: 40).
ASPECTS OF BIOLOGY. The full life-history of this species is not known. Chabaud & Campana- Rouget (1959) discovered some immature specimens of a lecithochiriine encapsulated in gobiid, labrid and blenniid teleosts in an aquarium at Banyuls-sur-Mer on the Mediterranean coast of France. In the same aquarium they found a cystophorous cercaria in the top-shell Gibbula varia, which they thought to be identical with Cercaria vaullegeardi Pelseneer, 1906. This is an unusual cystophorous cercaria in that it apparently arises from a daughter-sporocyst rather than a redia,
64 D. I. GIBSON & R. A. BRAY
which is the normal occurrence in hemiuroids. Nevertheless, according to Matthews (1980), this type of daughter-sporocyst is a modified redia, as the birth-pore and birth-canal of the former are homologous with the mouth, pharynx and caecum of the latter. Although Chabaud & Campana- Rouget failed to find copepods infested with the metacercariae, they assumed that these cercariae were the larval form of the encapsulated, immature forms from fishes. Knowing that L.fusiforme occurred locally in Conger conger, they assumed that these encapsulated forms were immature specimens of the latter species, and thus formed the missing link between the metacercariae in copepods and the adults in congers. Unfortunately, there was no direct evidence for this relation- ship, and, considering both the sucker-ratio in the figure of Chabaud & Campana-Rouget (1959) and the work of Carrere (1938), these encysted forms are perhaps more likely to have been L. rufoviride. The records of Cercaria vaullegeardi from our region are given on p. 000, although it is likely that there has been some confusion between the larval forms of different species, as there are small differences between the descriptions. It does seem likely, however, that some of the records of C. vaullegeardi refer to the larval stage of L. rufoviride, although we have biochemical data (see Gibson, Rollinson & Matthews, 1985) which indicate that C. vaullegeardi of Matthews (1980, 198 la A 19826) is L.furcolabiatum.
Similarly, the records of encapsulated forms, which may be progenetic, from the viscera of various fishes, such as gobiids and labrids, may also refer to a mixture of species, although it seems likely that many are L. rufoviride. In the region of the SW British Isles, however, many of the records, especially those from rock-pool fishes, are L. furcolabiatum. Similar young, usually immature, worms may be found in the stomach or intestine of a wide variety of teleosts; but these are, presumably, either accidental infestations which have been recently ingested or specimens en route to the body-cavity and re-encapsulation.
Other work on this topic includes the early comments of Looss (1908), who mentioned that the young form of 'L. gravidum' occurs encapsulated in labrids, Syngnathus acus, Hippocampus ramulosus and other fishes at Trieste, and Carrere (1938), who claimed to have fed some encapsu- lated specimens from Gobius niger to the frog Hyla arborea and to have recovered worms in good condition with some development of the gonads after three days. Carrere also infested specimens of Pomatoschistus minutus with cysts from Symphodus cinereus and obtained ovigerous worms. These results are, however, questionable, for, as mentioned above, the encapsulated worms are often ovigerous.
The normal definitive host of this species is Conger conger, but, especially in the northern part of its range where congers are less common, it also occurs commonly in Anguilla anguilla. It has also been recorded at Plymouth in the stomach of Lophius piscatorius. We have examined three specimens collected from this host at Plymouth and can confirm that they are relatively large and ovigerous, although perhaps containing fewer eggs than similar sized specimens from congers. Although it is possible that L. rufoviride might survive in L. piscatorius, this is not certain, as specimens could be acquired accidentally if this fish preys upon eels or small fishes harbouring progenetic encapsulated worms.
In summary, therefore, the life-history appears to be as follows: (1) mother-sporocyst and daughter-parthenitae (producing (?) Cercaria vaullegeardi) in Gibbula; (2) metacercariae in copepods; (3) small, encapsulated, immature (but occasionally ovigerous) forms on viscera of small planktivorous fishes; and (4) mature adults in eels.
The distribution of this species appears to be Lusitanean, probably mimicking its major definitive host, C. conger, as it occurs in the Mediterranean Sea and the eastern coast of the North Atlantic between the Canaries and Bergen, Norway (we have recorded an encapsulated specimen, probably of this species, off the Faeroes). The absence of C. conger in the Black Sea presumably explains the absence of definitive records of this species from that region. It is worth noting that Sey (1970) reported this species from another congrid, Ariosoma balearicum, in the Adriatic Sea.
PREVIOUS DESCRIPTIONS. Dujardin (1845: 421; as Distoma rufoviride; brief); Wagener (1860: 178; as D. rufoviride; figured); Olsson (1868: 49; as D. rufoviride; brief); Juel (1889: 6; as Apoblema rufoviride; terminal genitalia); Johnstone (1907: 277; as Distomum ocreatuni); Looss (1908: 144; as
HEMIURIDAE 65
L. rufoviride and L. gravidum; detailed); Timon-David (1937: 19; as L. rufoviride and L. gravidum; brief); D.O. Jones (1943: 47; detailed); Dawes (1947: 287); Janiszewska (1953: 29).
DESCRIPTION (Figs 12, 13, 16A,B, 17F). This description is based upon 40 whole-mounted and four sectioned specimens from Conger conger and Anguilla anguilla. The body of this worm is fusiform, its breadth depending upon the state of contraction. Flattened specimens may be up to twice the size of similar unflattened worms and vary in shape from fusiform to oval. Although generally quite large for a hemiruid, there is often a relatively wide range of sizes found: see Table 9 for the measurements of this species. The ecsoma in preserved specimens is usually, but not always, withdrawn, although it often protrudes slightly in flattened material. The body surface is smooth. The large oral sucker is ventrally subterminal, being surmounted by a distinct pre-oral lobe which may be squared off. A regular arrangement of papillae occur surrounding the oral sucker (Fig. 16A,B), but these are usually difficult to discern. Within the postero-lateral regions of the wall of the oral sucker are two distinct, symmetrical thickenings which protrude into the lumen (Figs 12, 13, 16A,B). A less obvious thickening also occurs in the anterior wall of this sucker. The spherical ventral sucker is slightly larger than the oral sucker, the ratio usually being in the region of 1 : 1 -2-1 -6, and is situated at about one-third of the body-length from the anterior^ end. A small presomatic pit is present between the genital pore and the anterior margin of the ventral sucker (Fig. 13B,E), but this is often difficult to see in whole-mounts.
There is no prepharynx, but a small (in relation to the size of the oral sucker) pharynx gives rise to a distinct, short and sac-like oesophagus. The oesophagus opens posteriorly, postero-dorsally or dorsally, depending upon the state of contraction, via a sphincter into a short commissure which extends between the two gut-caeca. The commissure almost immediately dilates laterally on each side to form a distinct 'Driisenmagen'. From these the caeca extend laterally, antero- laterally or postero-laterally and then curve to run posteriorly in the lateral or dorso-lateral fields. At about the 'shoulder-region' the caeca normally become much wider than they were initially. They end blindly close to the proximal end of the ecsoma or occasionally inside the proximal end of this organ when it is extruded.
The excretory pore occurs terminally on the ecsoma. It leads into the stout stem of a tubular, Y-shaped excretory vesicle, which passes forward medially and bifurcates at about the level of the testes. The two narrow arms pass into the forebody laterally and unite dorsally to the oral sucker.
The two oval testes occur ventro-laterally and symmetrically or slightly obliquely close to the posterior margin of the ventral sucker. They are normally widely separated. The two vasa efferentia unite as they meet the thin wall of the proximal end of the seminal vesicle. The latter organ is essentially bipartite, but often appears to be tripartite (Fig. 13B). Its proximal part is large, but variable in size, elongate-saccular and is often curved, folded or constricted such that it appears to be divided with a small, distinct distal region. The distal part of the seminal vesicle